HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) All Versions of this Article: 289/2/R514    most recent 00036.2005v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (10) Citing Articles via Google Scholar Google Scholar Articles by Shi, H. Articles by Bartness, T. J. Search for Related Content PubMed PubMed Citation Articles by Shi, H. Articles by Bartness, T. J.

APPETITE, OBESITY, DIGESTION, AND METABOLISM

White adipose tissue sensory nerve denervation mimics lipectomy-induced compensatory increases in adiposity

Department of Biology and Center for Behavioral Neuroscience, Georgia State University, Atlanta, Georgia

Submitted 19 January 2005 ; accepted in final form 25 April 2005

	ABSTRACT

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION GRANTS REFERENCES

 
The sensory innervation of white adipose tissue (WAT) is indicated by the labeling of sensory bipolar neurons in the dorsal root ganglion after retrograde dye placement into WAT. In addition, immunoreactivity (ir) for sensory-associated neuropeptides such as calcitonin gene-related peptide (CGRP) and substance P in WAT pads also supports the notion of WAT sensory innervation. The function of this sensory innervation is unknown but could involve conveying the degree of adiposity to the brain. In tests of total body fat regulation, partial surgical lipectomy triggers compensatory increases in the mass of nonexcised WAT, ultimately resulting in restoration of total body fat levels in Siberian hamsters and other animals. The signal that triggers this compensation is unknown but could involve disruption of WAT sensory innervation that accompanies lipectomy. Therefore, a local and selective sensory denervation was accomplished by microinjecting the sensory nerve neurotoxin capsaicin bilaterally into epididymal WAT (EWAT) of Siberian hamsters, whereas controls received vehicle injections. Additional hamsters had bilateral EWAT lipectomy (EWATx) or sham lipectomy. As seen previously, EWATx resulted in significantly increased retroperitoneal WAT (RWAT) and inguinal WAT (IWAT) masses. Capsaicin treatment significantly decreased CGRP- but not tyrosine hydroxylase-ir, attesting to the diminished and selective sensory innervation. Capsaicin-treated hamsters also had increased RWAT and, to a lesser degree, IWAT mass largely mimicking the WAT mass increases seen after lipectomy. Collectively, these data suggest the possibility that information related to peripheral lipid stores may be conveyed to the brain via the sensory innervation of WAT.

capsaicin; calcitonin gene-related peptide; obesity; hamster

The response to lipectomy is pervasive across species occurring in laboratory rats and mice, as well as in species that undergo seasonal or circannual fluctuations in body fat content, such as ground squirrels and Syrian hamsters and Siberian hamsters (Phodopus sungorusI), our species of study here (for a review, see Ref. 25). These compensatory increases in WAT pad mass ultimately result in restoration of total body fat levels and occur without changes in food intake (for a review, see Ref. 25). Although much still remains to be known regarding the mechanisms underlying the compensatory responses to the lipid deficit that ultimately replenish total body fat levels, here, we focus on determining the signal that initiates the compensatory responses.

An obvious circulating factor that could trigger the lipectomy-induced increases in body fat is leptin, the largely adipose-derived cytokine thought of as a conveyor of body fat levels to the brain (for a review, see Ref. 37). It does not appear, however, that leptin is necessary for the lipectomy-induced stimulation of lipid accumulation by the nonexcised WAT pads because animals with nonfunctional leptin signaling (ob/ob and db/db mice) recover lipectomy-induced body fat losses despite not having leptin or leptin receptors (13). Alternatively, the trigger for lipectomy-induced body fat compensation could be neural. WAT has sensory innervation, as first demonstrated by tract tracing (10). Specifically, implantation of the retrograde tract tracer, true blue, into laboratory rat WAT pads labels bipolar sensory neurons in the dorsal root ganglia (10). In addition, WAT contains immunoreactivity (ir) for sensory-associated neuropeptides such as substance P and calcitonin gene-related peptide (CGRP; 11, 33). Although the exact function of the sensory innervation of WAT is unknown (for a review, see Refs. 2 and 3), the neuroanatomical evidence for its presence is strong.

Therefore, to begin to determine the functions of WAT sensory innervation, we tested the possibility that WAT sensory innervation informs the central nervous system of peripheral lipid stores. Specifically, we tested whether bilateral epididymal WAT (EWAT) sensory denervation triggers increases in the mass of intact WAT pads analogous to the increases in the mass of nonexcised WAT pads after EWAT lipectomy (EWATx) (e.g., Refs. 19, 22, 23). Intra-WAT pad microinjections of capsaicin, a sensory neurotoxin (14), were used to denervate EWAT locally and selectively, as we have described previously (33).

	MATERIALS AND METHODS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION GRANTS REFERENCES

 
Animals and Housing Conditions

Our Siberian hamster (Phodopus sungorus) colony was established in 1988, and its genealogy has been described recently (6). Hamsters were exposed to a long summer-like day (16:8-h light-dark cycle with lights on at 0300 EST). Room temperature at 20°C, and relative humidity was maintained at 50 ± 5% throughout the experiment. All animals had ad libitum access to Purina Rodent Diet (#5001) and tap water. All experimental procedures were approved by the Georgia State University Institutional Animal Care and Use Committee in accordance with Public Health Service and United States Department of Agriculture guidelines.

Does Sensory Denervation Trigger Lipectomy-Like Increases in WAT Mass Similar to That Seen After Lipectomy?

Experimental design. Sixty, 3-mo-old adult male Siberian hamsters were obtained from our breeding colony and divided into groups matched for body mass and percent body mass change after a 2-wk single-housing adaptation period, during which they were weighed once each week (n = 10 hamsters/group). Each group received one of the following treatments: bilateral EWAT sham lipectomy (Sham EWATx), bilateral EWATx, bilateral EWAT Sham denervation (Sham Den), bilateral surgical denervation [Surg Den; disrupting both sensory and sympathetic nervous system (SNS) innervation], bilateral EWAT treatment with vehicle, or capsaicin, a sensory neurotoxin (14) that disrupts sensory but not SNS innervation (33). Body mass and food intake were measured weekly to the nearest 0.01 g for 12 wk, a time when compensation for lipectomy-induced lipid deficits is complete (e.g., 19, 23). At the end of this experiment, the animals were killed and fat pads were harvested, weighed, and processed for histological verification of the denervation procedure (see below).

General surgical procedures. Hamsters were anesthetized with pentobarbital sodium (50 mg/kg ip) for all surgeries. The hair was removed from the incision area and then the area was wiped with 50% ethanol-soaked gauze. A single abdominal midline incision was made, through which bilateral EWAT pads could be accessed and care in the depth of the incision was taken to avoid the underlying blood vessels and musculature. Fat pads were kept moist with 0.15 M NaCl-soaked gauze. After the surgeries, the abdominal peritoneum was closed with sterile silk sutures, and the skin was closed with sterile wound clips. Nitrofurozone powder was applied to the incision site surface to decrease the incidence of infection.

Surgical lipectomy. For EWATx, pads were excised with care taken to avoid damage to the testicular blood supply, as described previously (19, 23, 33). Sham EWATx surgery consisted of fat pad manipulation, in which both left and right EWAT pads were lifted out of the peritoneal cavity intact and then replaced.

Surgical denervation. Surgical denervation was performed as we described previous (33). Briefly, a drop of 1% toluidine blue was applied to the EWAT pads to facilitate visualization of the nerves. The nerves were then freed from the surrounding tissue and vasculature to minimize disturbances in the blood flow and cut in two or more places. For Sham Den surgery, fat pads were gently lifted or pushed with tissue forceps to visualize the nerves without damaging either the nerves or the blood vessels. After surgery, the denervated or sham-denervated pads were replaced back to their original locations.

Chemical sensory denervation. The WAT pads were sensory denervated using our previously described procedure (33). Briefly, the EWAT pads for hamsters in the Capsaicin group were injected with 20 microinjections (2 µl per injection) of 20 µg/µl of capsaicin (Sigma Chemical, St. Louis, MO) dissolved in 10% of ethanol, 10% of Tween 80 and 80% of 0.9% NaCl, whereas the sham pads (Vehicle) received the same volume and numbers of injections of the vehicle. The dose of capsaicin was based on the lowest effective dose that significantly decreased CGRP-ir in pilot studies and used previously to demonstrate the presence of capsaicin-sensitive nerves in WAT (33). Reflux of the solutions was reduced by holding the needle at each injection site for 60 s before removing the microsyringe. The capsaicin and vehicle injections were placed so as to cover the full extent of the pads.

Tissue harvesting. Twelve weeks after surgery, animals were deeply anesthetized with pentobarbital sodium (80 mg/kg ip) and perfused transcardially with 100 ml of saline followed by 150 ml of 4% paraformaldehyde in 0.1 M phosphate buffer solution (pH = 7.4). EWAT, inguinal WAT (IWAT), retroperitoneal WAT (RWAT), and dorsal subcutaneous WAT (DWAT) were harvested and weighed. Testes also were removed and weighed as an indicator of reproductive status. The treated EWAT pads were stored in 4% paraformaldehyde until processing for immunohistochemical quantification (see Immunohistochemistry and quantitative microscopy) of tyrosine hydroxylase (TH) and CGRP-ir to verify chemical sensory or surgical denervations. Positive control tissues (ventral medulla for TH and skeletal muscle for CGRP) also were run.

Immunohistochemistry and quantitative microscopy. Immunohistochemistry for TH- and CGRP-ir was performed on WAT using the avidin-biotin complex peroxidase method, according to the method of Giordano et al. (11). Primary polyclonal antibodies [1:300] mouse anti-TH (Chemicon International, Temecula, CA) or [1:500] mouse anti-CGRP (Chemicon International) were used, and antibody specificity was demonstrated by incubating sections without the primary antibody and by preadsorption of the primary antibody with its antigen; each procedure resulted in neither TH-ir nor CGRP-ir. The presence of TH-ir or CGRP-ir using the above specific primary antibodies indicated the presence of sympathetic or sensory nerves, respectively, and was considered as a positive staining.

Surgical and chemical denervations were verified by quantifying TH-ir and CGRP-ir using our previously described methodology (33) with the researcher blind to the treatment of the pad. Briefly, WAT pads were continuously sectioned and grouped at 200-µm intervals. Two slides were randomly chosen from each interval and used for immunohistochemistry to localize the TH-ir and CGRP-ir. For each slice on each of these slides, TH-ir and CGRP-ir were quantified from five parenchymal fields. This was accomplished by first viewing each slide to determine how many areas showed positive staining for any given section. If more than five areas with positive staining were found, the first five encountered were used. If less than five areas with positive staining were found, then another slide was chosen or, if this were not possible (many slides from denervated WAT had one or two areas of positive staining), then any areas with positive staining on the two slides were chosen. The average numbers of TH-ir and CGRP-ir were compared between groups.

Statistical analyses. Weekly body mass and food intake were analyzed using repeated-measures ANOVA [SigmaStat 2.0, San Rafael, CA; treatment x time (6 x 12)]. Two-way ANOVA (SigmaStat 2.0) was used to analyze terminal measures of tissue mass [treatment x pad (6 x 4)] and TH-ir or CGRP-ir [treatment x peptide (6 x 2)]. Differences between means were considered statistically significant if P < 0.05. Exact probabilities and test values were omitted for simplicity and clarity of the presentation of the results.

	RESULTS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION GRANTS REFERENCES

 
Does Sensory Denervation Trigger Lipectomy-Like Increases in WAT Mass Similar to That Seen After Lipectomy?

Three of the ten Capsaicin animals, 3 of the 10 Surg Den animals and 2 of the 10 EWATx animals either died or appeared unhealthy during the immediate postsurgical recovery period and therefore were euthanized and excluded from study yielding final group numbers of n = 7, n = 7 and n = 8, respectively. All control animals survived (n = 10 per group), and all surviving animals from all groups were healthy, as indicated by their body mass increase and food intakes (see below).

Body mass and food intake. Body mass was not significantly affected by any treatment (Figs. 1A, 2A, and 3A). EWATx animals decreased food intake for the first 2 wk after surgery compared with that for Sham EWATx-treated animals (P < 0.05; Fig. 1B). Food intake was not significantly different between the Capsaicin and Vehicle groups (Fig. 2B). Food intake was significantly decreased in Surg Den hamsters the first week after surgical denervation compared with Sham Den animals (Fig. 3B). Food intakes for the remaining weeks, as well as cumulative food intake, however, were not different among the groups (Figs. 1B, 2B, and 3B).

View larger version (20K): [in this window] [in a new window]   Fig. 1. Means ± SE weekly body mass (A), weekly food intake and cumulative food intake (B) for hamsters that underwent bilateral epididymal white adipose tissue removal (EWATx) or Sham lipectomy (Sham EWATx). *P < 0.05 EWATx vs. Sham EWATx.

View larger version (20K): [in this window] [in a new window]   Fig. 2. Means ± SE weekly body mass (A), weekly food intake and cumulative food intake (B) for hamsters that underwent bilateral epididymal white adipose tissue capsaicin treatment (Capsaicin) or vehicle treatment (Vehicle).

View larger version (20K): [in this window] [in a new window]   Fig. 3. Means ± SE weekly body mass (A), weekly food intake and cumulative food intake (B) for hamsters that underwent bilateral epididymal white adipose tissue surgical denervation (Surg Den) or sham denervation (Sham Den). *P < 0.05 Surg Den vs. Sham Den.

View larger version (14K): [in this window] [in a new window]   Fig. 4. Means ± SE fat pad mass for retroperitoneal white adipose tissue (RWAT; top) and inguinal white adipose tissue (IWAT; bottom) of hamsters that underwent epididymal white adipose tissue (EWAT) capsaicin, surgical denervation, or lipectomy treatment. Dissimilar letters are significantly different from one another (P < 0.05).

View larger version (14K): [in this window] [in a new window]   Fig. 5. Means ± SE fat pad mass dorsosubcutaneous white adipose tissue (DWAT; top) and epididymal white adipose tissue (EWAT; bottom) of hamsters that underwent EWAT capsaicin, surgical denervation, or lipectomy treatment. Dissimilar letters are significantly different from one another (P < 0.05).

EWAT histology. Consistent with our previous study (33), CGRP-ir (P < 0.05; Fig. 6A), but not TH-ir, was significantly decreased in the Capsaicin compared with Vehicle WAT documenting disruption of sensory, but not sympathetic innervation of EWAT. Similar to our previous study (33), surgical denervation of EWAT (Surg Den) significantly decreased both CGRP-ir and TH-ir compared with control EWAT (Sham Den; P < 0.05; Fig. 6B), suggesting disruption of both sensory and sympathetic innervations.

View larger version (15K): [in this window] [in a new window]   Fig. 6. Means ± SE numbers of calcitonin gene-related peptide (CGRP)- and tyrosine hydroxylase (TH)-immunoreactive (ir) sites of the vehicle-treated epididymal white adipose tissue (EWAT; Vehicle) and capsaicin-treated EWAT (Capsaicin) (A) and sham-denervated EWAT (Sham Den) and surgically denervated EWAT (Surg Den) (B). *P < 0.05 Vehicle vs. Capsaicin or Sham Den vs. Surg Den.

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION GRANTS REFERENCES

Surgical denervation, in which both the sympathetic and sensory innervations of WAT are at least partially destroyed (present study; Ref. 33), did not trigger increased RWAT or IWAT mass. Because surgical denervation significantly decreased CGRP-ir to the same or greater extent as capsaicin treatment (present study and Ref. 33) and then if the signal for triggering lipectomy- (e.g., 19, 21, 23, 32) and capsaicin-induced increases in intact WAT growth is sensory nerve disruption, one would expect surgical denervation-induced increases in intact pad growth. This lack of growth by the nonsurgically denervated WAT pads seems to be explained by another effect of WAT surgical denervation—the near doubling of the denervated WAT pad mass [50% increase after surgical denervation of IWAT or RWAT (6, 7, 38), 30% increase for EWAT (present study and Ref. 33)] largely reflected as increases in fat cell number (e.g., Refs. 6, 33, 38). These sympathetic denervation-induced increases in fat cell number (6–8, 33, 38) have been attributed to removal of sympathetic inhibition of fat cell proliferation (15). Sensorydenervation, however, does not increase WAT mass or fat cell number (33). In the present study, the smaller increase in WAT mass after EWAT surgical denervation compared with that after IWAT or RWAT surgical denervation (6, 33, 38) seems to be due to the lesser propensity of the former pad for growth by adipocyte proliferation compared with the latter pads (e.g., Ref. 9). Thus the surgical denervation-induced increased accumulation of lipid by EWAT in the present study likely inhibited lipid accumulation by nonsurgically denervated WAT pads.

If the sensory innervation of WAT conveys body fat information to the brain, then what is the nature of the lipid-associated signal? Quite simply, this is not known, but some possibilities exist (for a review, see Refs. 2 and 3). One possibility would be that a factor associated with lipid storage or mobilization may roughly correlate with body fat levels and, in its absence, would trigger responses leading to compensation by other lipid depots. For example, lipolysis results in the catabolism of triacylglycerols into free fatty acids and glycerol (27), and WAT sensory nerves could respond to changes in either or both, thereby providing the brain with some information as to the status of lipid storage in WAT depots (2). To our knowledge, the response of WAT sensory nerves to glycerol, free fatty acids, or for that matter, to any substance, has not been tested. Precedent exists, however, for sensory nerves responding to such signals because some gastrointestinal sensory nerves are activated by fatty acids (17, 26). Although the role of leptin in total body fat regulation has been questioned (see Introduction), leptin appears capable of activating WAT sensory nerves (28). That is, direct injections of leptin into the EWAT of laboratory rats increases sensory nerve firing rates (28), suggesting that leptin may act as a paracrine rather than a circulating factor to convey adiposity information to the brain via a neural sensory conduit.

Finally, although we found that, testes mass was significantly decreased in EWATx hamsters compared with their Sham EWATx controls, testes of this diminished size are still fully functional with regard to serum testosterone concentrations (20). This is important because testosterone affects body and lipid mass in this species (1, 4, 34); however, unlike laboratory rats and mice, decreases in serum testosterone are associated with decreases in body fat in Siberian hamsters (for a review, see Ref. 35). Thus any inadvertent damage to the testes during EWAT manipulations would decrease testosterone and tend to oppose the compensatory increases in WAT pad mass that accompanies lipectomy and capsaicin treatment.

In summary, the exact roles of sensory innervation of WAT are unknown, and the current study is a beginning toward a deeper understanding of its role in body fat regulation. The results of the present study show that capsaicin disruption of WAT sensory innervation triggers increases in noninjected WAT pads that are remarkably similar to the pattern and degree of body fat compensation that follows lipectomy, suggesting that sensory nerves convey adiposity levels to the brain.

	GRANTS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION GRANTS REFERENCES

 
This research was supported by National Institutes of Health R01-DK35254 and a Georgia State University Research Program Enhancement award to T. J. Bartness.

	ACKNOWLEDGMENTS

 
We thank Dr. Ruth Harris for her critical reading of the manuscript and discussions of these results, Walliar Rahman and Nicole Rankine for assistance in data collection, and Qiujiang W. Po for expert animal care.

	FOOTNOTES

 

Address for reprint requests and other correspondence: T. J. Bartness, Dept. of Biology, Georgia State Univ., 24 Peachtree Center Ave., NE, Atlanta, GA 30302–4010 (E-mail: bartness{at}gsu.edu)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

	REFERENCES

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION GRANTS REFERENCES

 

1. Bartness TJ. Photoperiod, sex, gonadal steroids and housing density affect body fat in hamsters. Physiol Behav 60: 517–529, 1996.[Medline]
2. Bartness TJ and Bamshad M. Innervation of mammalian white adipose tissue: Implications for the regulation of total body fat. Am J Physiol Regul Integr Comp Physiol 275: R1399–R1411, 1998.[Abstract/Free Full Text]
3. Bartness TJ, Demas GE, and Song CK. Central nervous system innervation of white adipose tissue. In: Adipose Tissue, edited by Klaus S. Georgetown, TX: Landes Bioscience, 2001, p. 116–130.
4. Bartness TJ, Elliott JA, and Goldman BD. Control of torpor and body weight patterns by a seasonal timer in Siberian hamsters. Am J Physiol Regul Integr Comp Physiol 257: R142–R149, 1989.[Abstract/Free Full Text]
5. Bjorntorp P, Kral JG, Lundholm K, Presta E, Walks D, and Yang MU. Refeeding after fasting in the rat: energy substrate fluxes and replenishment of energy stores. Am J Clin Nutr 36: 450–456, 1982.[Abstract/Free Full Text]
6. Bowers RR, Festuccia WTL, Song CK, Shi H, Migliorini RH, and Bartness TJ. Sympathetic innervation of white adipose tissue and its regulation of fat cell number. Am J Physiol Regul Integr Comp Physiol 286: R1167–R1175, 2004.[Abstract/Free Full Text]
7. Cousin B, Casteilla L, Lafontan M, Ambid L, Langin D, Berthault MF, and Penicaud L. Local sympathetic denervation of white adipose tissue in rats induces preadipocyte proliferation without noticeable changes in metabolism. Endocrinology 133: 2255–2262, 1993.[Abstract/Free Full Text]
8. Demas GE and Bartness TJ. Novel method for localized, functional sympathetic nervous system denervation of peripheral tissue using guanethidine. J Neurosci Methods 112: 21–28, 2001.[CrossRef][Web of Science][Medline]
9. DiGirolamo M, Fine JB, Tagra K, and Rossmanith R. Qualitative regional differences in adipose tissue growth and cellularity in male Wistar rats fed ad libitum. Am J Physiol Regul Integr Comp Physiol 274: R1460–R1467, 1998.[Abstract/Free Full Text]
10. Fishman RB and Dark J. Sensory innervation of white adipose tissue. Am J Physiol Regul Integr Comp Physiol 253: R942–R944, 1987.[Abstract/Free Full Text]
11. Giordano A, Morroni M, Santone G, Marchesi GF, and Cinti S. Tyrosine hydroxylase, neuropeptide Y, substance P, calcitonin gene-related peptide and vasoactive intestinal peptide in nerves of rat periovarian adipose tissue: an immunohistochemical and ultrastructural investigation. J Neurocytol 25: 125–136, 1996.[CrossRef][Web of Science][Medline]
12. Harris RB, Kasser TR, and Martin RJ. Dynamics of recovery of body composition after overfeeding, food restriction or starvation of mature female rats. J Nutr 116: 2536–2546, 1986.[Abstract/Free Full Text]
13. Harris RBS, Hausman DB, and Bartness TJ. Compensation for partial lipectomy in mice with genetic alterations of leptin and its receptor subtypes. Am J Physiol Regul Integr Comp Physiol 283: R1094–R1103, 2002.[Abstract/Free Full Text]
14. Jansco G, Kiraly E, Joo F, Such G, and Nagy A. Selective degeneration by capsaicin of a subpopulation of primary sensory neurons in the adult rat. Neurosci Lett 59: 209–214, 1985.[CrossRef][Web of Science][Medline]
15. Jones DD, Ramsay TG, Hausman GJ, and Martin RJ. Norepinephrine inhibits rat preadipocyte proliferation. Int J Obes 16: 349–354, 1992.[Web of Science][Medline]
16. Kennedy GC. The role of depot fat in the hypothalamic control of food intake in the rat. Proc R Soc Lond B Biol Sci 140: 578–592, 1953.[Medline]
17. Lal S, Kirkup AJ, Brunsden AM, Thompson DG, and Grundy D. Vagal afferent responses to fatty acids of different chain length in the rat. Am J Physiol Gastrointest Liver Physiol 281: G907–G915, 2001.[Abstract/Free Full Text]
18. Ma SW and Foster DO. Starvation-induced changes in metabolic rate, blood flow and regional energy expenditure in rats. Can J Physiol Pharmacol 64: 1252–1258, 1986.[Web of Science][Medline]
19. Mauer MM and Bartness TJ. Body fat regulation following partial lipectomy in Siberian hamsters is photoperiod-dependent and fat pad-specific. Am J Physiol Regul Integr Comp Physiol 266: R870–R878, 1994.[Abstract/Free Full Text]
20. Mauer MM and Bartness TJ. A role for testosterone in the maintenance of seasonally-appropriate body mass, but not in lipectomy-induced body fat compensation in Siberian hamsters. Obesity Res 3: 31–41, 1995.[Web of Science][Medline]
21. Mauer MM and Bartness TJ. Temporal changes in fat pad mass following lipectomy in Siberian hamsters. Physiol Behav 62: 1029–1036, 1997.[CrossRef][Medline]
22. Mauer MM and Bartness TJ. Photoperiod-dependent fat pad mass and cellularity changes following partial lipectomy in Siberian hamsters. Am J Physiol Regul Integr Comp Physiol 270: R383–R392, 1996.[Abstract/Free Full Text]
23. Mauer MM and Bartness TJ. Fat pad-specific compensatory mass increases after varying degrees of partial lipectomy in Siberian hamsters. Am J Physiol Regul Integr Comp Physiol 273: R2117–R2123, 1997.[Abstract/Free Full Text]
24. Mauer MM and Bartness TJ. Short day-like body mass changes do not prevent fat pad compensation after lipectomy in Siberian hamsters. Am J Physiol Regul Integr Comp Physiol 272: R68–R77, 1997.[Abstract/Free Full Text]
25. Mauer MM, Harris RBS, and Bartness TJ. The regulation of total body fat: lessons learned from lipectomy studies. Neurosci Biobehav Rev 25: 15–28, 2001.[CrossRef][Web of Science][Medline]
26. Melone J. Vagal receptors sensitive to lipids in the small intestine of the cat. J Auton Nerv Syst 17: 231–241, 1986.[CrossRef][Web of Science][Medline]
27. Newsholme EA and Leech AR. Biochemistry for the Medical Sciences. Chichester, UK: John Wiley, 1983.
28. Niijima A. Reflex effects from leptin sensors in the white adipose tissue of the epididymis to the efferent activity of the sympathetic and vagus nerve in the rat. Neurosci Lett 262: 125–128, 1999.[CrossRef][Web of Science][Medline]
29. Penicaud L and LeMagnen J. Recovery of body weight following starvation or food restriction in rats. Neurosci Biobehav Rev 4: 47–52, 1980.
30. Saito M, Minokoshi Y, and Shimazu T. Metabolic and sympathetic nerve activities of brown adipose tissue in tube-fed rats. Am J Physiol Endocrinol Metab 257: E374–E378, 1989.[Abstract/Free Full Text]
31. Schneider JE and Wade GN. Decreased availability of metabolic fuels induces anestrus in golden hamsters. Am J Physiol Regul Integr Comp Physiol 258: R750–R755, 1990.[Abstract/Free Full Text]
32. Shi H, Bowers RR, and Bartness TJ. Norepinephrine turnover in brown and white adipose tissue after partial lipectomy. Physiol Behav 81: 535–543, 2004.[CrossRef][Medline]
33. Shi H, Song CK, Giordano A, Cinti S, and Bartness TJ. Sensory or sympathetic white adipose tissue denervation differentially affects depot growth and cellularity. Am J Physiol Regul Integr Comp Physiol 288: R1028–R1037, 2005.[Abstract/Free Full Text]
34. Vitale PM, Darrow JM, Duncan MJ, Shustak CA, and Goldman BD. Effects of photoperiod, pinealectomy and castration on body weight and daily torpor in Djungarian hamsters (Phodopus sungorus). J Endocrinol 106: 367–375, 1985.[Abstract/Free Full Text]
35. Wade GN, Gray JM, and Bartness TJ. Gonadal influences on adiposity. Int J Obes 9: 83–92, 1985.
36. Wood AD and Bartness TJ. Partial lipectomy, but not PVN lesions, increases food hoarding by Siberian hamsters. Am J Physiol Regul Integr Comp Physiol 272: R783–R792, 1997.[Abstract/Free Full Text]
37. Woods SC, Seeley RJ, Porte DJr, and Schwartz MW. Signals that regulate food intake and energy homeostasis. Science 280: 1378–1383, 1998.[Abstract/Free Full Text]
38. Youngstrom TG and Bartness TJ. White adipose tissue sympathetic nervous system denervation increases fat pad mass and fat cell number. Am J Physiol Regul Integr Comp Physiol 275: R1488–R1493, 1998.[Abstract/Free Full Text]

This article has been cited by other articles:

				M. E. Dailey and T. J. Bartness Fat pad-specific effects of lipectomy on foraging, food hoarding, and food intake Am J Physiol Regulatory Integrative Comp Physiol, February 1, 2008; 294(2): R321 - R328. [Abstract] [Full Text] [PDF]

				A. Giordano, C. Kay Song, R. R. Bowers, J. Christopher Ehlen, A. Frontini, S. Cinti, and T. J. Bartness Reply to Kreier and Buijs: no sympathy for the claim of parasympathetic innervation of white adipose tissue Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2007; 293(1): R550 - R552. [Full Text] [PDF]

				H. Shi, A. D. Strader, S. C. Woods, and R. J. Seeley Sexually dimorphic responses to fat loss after caloric restriction or surgical lipectomy Am J Physiol Endocrinol Metab, July 1, 2007; 293(1): E316 - E326. [Abstract] [Full Text] [PDF]

				M. T. Foster and T. J. Bartness Sympathetic but not sensory denervation stimulates white adipocyte proliferation Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2006; 291(6): R1630 - R1637. [Abstract] [Full Text] [PDF]

				A. Giordano, C. K. Song, R. R. Bowers, J. C. Ehlen, A. Frontini, S. Cinti, and T. J. Bartness White adipose tissue lacks significant vagal innervation and immunohistochemical evidence of parasympathetic innervation Am J Physiol Regulatory Integrative Comp Physiol, November 1, 2006; 291(5): R1243 - R1255. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) All Versions of this Article: 289/2/R514    most recent 00036.2005v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (10) Citing Articles via Google Scholar Google Scholar Articles by Shi, H. Articles by Bartness, T. J. Search for Related Content PubMed PubMed Citation Articles by Shi, H. Articles by Bartness, T. J.