Differential metabolism of brown adipose tissue in newborn rabbits in relation to position in the litter huddle

Journal of Thermal Biology

Volumn 51, Issue , 2015, Pages 33-41

  García Torres, Esmeralda ^a,b   Hudson, Robyn ^c   Castelán, Francisco ^a   Martínez Gómez, Margarita ^a,c   Bautista, Amando ^a  

^a CENTRO TLAXCALA DE BIOLOGÍA DE LA CONDUCTA   (Mexico)

^b UNIVERSIDAD VERACRUZANA   (Mexico)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Adipocytes; Brown adipose tissue; Development; Oryctolagus cuniculus; Thermoregulation; Triglycerides

Indexed keywords

TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY MASS; BROWN ADIPOSE TISSUE; COLD EXPOSURE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; FEMALE; GROWTH RATE; HISTOPATHOLOGY; LIPID STORAGE; LONG TERM EXPOSURE; MALE; NEWBORN; NEWBORN MORTALITY; NONHUMAN; PERINATAL DEVELOPMENT; PERINATAL PERIOD; RABBIT; SKIN TEMPERATURE; THERMAL EXPOSURE; THERMOGENESIS; THERMOREGULATION; TISSUE DISTRIBUTION; TISSUE METABOLISM; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; COMPETITIVE BEHAVIOR; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY;

ORYCTOLAGUS CUNICULUS;

ADIPOSE TISSUE, BROWN; ANIMALS; ANIMALS, NEWBORN; COMPETITIVE BEHAVIOR; FEMALE; MALE; RABBITS; THERMOGENESIS; TRIGLYCERIDES;

EID: 84924801832     PISSN: 03064565     EISSN: 18790992     Source Type: Journal    
DOI: 10.1016/j.jtherbio.2015.03.003     Document Type: Article

References (59)

1. Bartelt A., Bruns O.T., Reimer R., Hohenberg H., Ittrich H., Peldschus K., Kaul M.G., Tromsdorf U.I., Weller H., Waurisch C., Eychmüller A., Gordts P.L.S.M., Rinninger F., Bruegelmann K., Freund B., Nielsen P., Merkel M., Heeren J. Brown adipose tissue activity controls triglyceride clearance. Nat. Med. 2011, 17:200-205.
2. Bartelt A., Merkel M., Heeren J. A new, powerful player in lipoprotein metabolism: brown adipose tissue. J. Mol. Med. 2012, 90:887-893.
3. Bautista A., Drummond H., Martínez-Gómez M., Hudson R. Thermal benefit of sibling presence in the newborn rabbit. Dev. Psychobiol. 2003, 43:208-215.
4. Bautista A., Mendoza-Degante M., Coureaud G., Martínez-Gómez M., Hudson R. Scramble competition in newborn domestic rabbits for an unusually restricted milk supply. Anim. Behav. 2005, 70:1011-1121.
5. Bautista A., García-Torres E., Martínez-Gómez M., Hudson R. Do newborn domestic rabbits Oryctolagus cuniculus compete for thermally advantageous position in the litter huddle?. Behav. Ecol. Sociobiol. 2008, 62:331-339.
6. Bautista A., García-Torres E., Prager G., Hudson R., Rödel H.G. Development of behavior in the litter huddle in rat pups: within- and between-litter differences. Dev. Psychobiol. 2010, 52:35-43.
7. Bautista A., Castelán F., Pérez-Roldán H., Martínez-Gómez M., Hudson R. Competition in newborn rabbits for thermally advantageous positions in the litter huddle is associated with individual differences in brown fat metabolism. Physiol. Behav. 2013, 118:189-194.
8. Bautista A., Rödel H.G., Monclús R., Juárez-Romero M., Cruz-Sánchez E., Martínez-Gómez M., Hudson R. Intrauterine position as a predictor of postnatal growth and survival in the rabbit. Physiol. Behav. 2015, 138:101-106.
9. Blumberg M.S., Sokoloff G. Thermoregulatory competence and behavioral expression in the young of altricial species-revisited. Dev. Psychobiol. 1998, 33:107-123.
10. Cannon B., Nedergaard J. Brown adipose tissue: functional and physiological significance. Physiol. Rev. 2004, 84:277-359.
11. Cannon B., Nedergaard J. Nonshivering thermogenesis and its adequate measurement in metabolic studies. J. Exp. Biol. 2011, 214:242-253.
12. Cao W.H., Madden C.J., Morrison S.F. Inhibition of brown adipose tissue thermogenesis by neurons in the ventrolateral medulla and in the nucleus tractus solitaries. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 299:R277-R290.
13. Coureaud G., Schaal B., Coudert P., Hudson R., Rideaud P., Orgeur P. Mimicking natural nursing conditions promotes early pup survival in domestic rabbits. Ethology 2000, 105:207-225.
14. Coureaud G., Schaal B., Coudert P., Rideaud P., Fortun-Lamothe L., Hudson R., Orgeur P. Immediate postnatal suckling in the rabbit: its influence on pup survival and growth. Reprod. Nutr. Dev. 2000, 40:19-32.
15. Dawkins M.J.R., Hull D. Brown adipose tissue and the response of new-born rabbits to cold. J. Physiol. 1964, 172:216-238.
16. Drummond H. Dominance in vertebrate broods and litters. Q. Rev. Biol. 2006, 81:3-32.
17. Drummond H., Vázquez E., Sánchez-Colón S., Martínez-Gómez M., Hudson R. Competition for milk in the domestic rabbit: survivors benefit from littermate deaths. Ethology 2000, 106:511-526.
18. Gilbert C., Blanc S., Giroud S., Trabalon M., Le Maho Y., Perret M., Ancel A. Role of huddling on the energetic of growth in a newborn altricial mammal. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293:R867-R876.
19. Gilbert C., McCafferty D.J., Giroud S., Ancel A., Blanc S. Private heat for public warmth: how huddling shapes individual thermogenic responses of rabbit pups. PLoS One 2012, 7:1-11.
20. Himms-Hagen J. Brown adipose tissue metabolism and thermogenesis. Ann. Rev. Nutr. 1985, 5:69-94.
21. Hudson R. Potential of the newborn rabbit for circadian rhythms research. Biol. Rhythm Res. 1998, 29:546-555.
22. Hudson R., Distel H. The pattern of behaviour of rabbit pups in the nest. Behaviour 1982, 79:255-271.
23. Hudson R., Distel H. Nipple location by newborn rabbits: behavioural evidence for pheromonal guidance. Behaviour 1983, 85:260-275.
24. Hudson R., Distel H. The temporal pattern of suckling in rabbit pups: a model of circadian synchrony between mother and young. Development of Circadian Rhythmicity and Photoperiodism in Mammals 1989, 83-102. Perinatology Press, Boston. S.M. Reppert (Ed.).
25. Hudson R., Müller A., Kennedy G.A. Parturition in the rabbit is compromised by daytime nursing: the role of oxytocin. Biol. Reprod. 1995, 53:519-524.
26. Hudson R., Trillmich F. Sibling competition and cooperation in mammals: challenges, developments and prospects. Behav. Ecol. Sociobiol. 2008, 62:299-307.
27. Hudson R., Bautista A., Reyes-Meza V., Morales Montor J., Rödel H.G. The effect of siblings on early development: a potential contributor to personality differences in mammals. Dev. Psychobiol. 2011, 53:564-574.
28. Hudson R., Maqueda B., Moctezuma J.V., Miranda A.M., Rödel H.G. Individual differences in testosterone and corticosterone levels in relation to early postnatal development in the rabbit Oryctolagus cuniculus. Physiol. Behav. 2011, 105:336-341.
29. Hull D. Oxygen consumption and body temperature of new-born rabbits and kittens exposed to cold. J. Physiol. 1965, 177:192-202.
30. Hull D., Segall M.M. The contribution of brown adipose tissue to heat production in the new-born rabbit. J. Physiol. 1965, 181:449-457.
31. Hull D., Segal M.M. Heat production in the new-born rabbit and the fat content of the brown adipose tissue. J. Physiol. 1965, 181:468-477.
32. Jilge B., Hudson R. Diversity and development of circadian rhythms in the European rabbit. Chronobiol. Int. 2001, 18:1-26.
33. Koolhaas J.M., Korte S.M., De Boer S.F., Van Der Vegt B.J., Van Reenen C.G., Hopster H., De Jong I.C., Ruis M.A.W., Blokhuis H.J. Coping styles in animals: current status in behaviour and stress-physiology. Neurosci. Biobehav. Rev. 1999, 23:925-935.
34. Lewejohann L., Zipser B., Sachser N. "Personality" in laboratory mice used for biomedical research: a way of understanding variability?. Dev. Psychobiol. 2011, 53:624-630.
35. Liang H., Ward W.F. PGC-1alpha: a key regulator of energy metabolism. Adv. Physiol. Educ. 2006, 30:145-151.
36. Loncar D. Development of thermogenic adipose tissue. Int. J. Dev. Biol. 1991, 35:321-333.
37. Mock D.W., Parker G.A. The Evolution of Sibling Rivalry 1997, Oxford University Press, Oxford.
38. Morrison S.F., Ramamurthy S., Young J.B. Reduced rearing temperature augments responses in sympathetic outflow to brown adipose tissue. J. Neurosci. 2000, 20:9264-9271.
39. Muciño E., Bautista A., Jiménez I., Martínez-Gómez M., Hudson R. Differential development of body equilibrium among littermates in the newborn rabbit. Dev. Psychobiol. 2009, 51:24-33.
40. Nicolás L., Martínez-Gómez M., Hudson R., Bautista A. Littermate presence enhances motor development, weight gain and competitive ability in newborn and juvenile domestic rabbits. Dev. Psychobiol. 2011, 53:37-46.
41. Pacheco-Cobos L., Rosetti M., Distel H., Hudson R. To stay or not to stay: the contribution of tactile and thermal cues to coming to rest in newborn rabbits. J. Comp. Physiol. A 2003, 189:383-389.
42. Reyes-Meza V., Hudson R., Martínez-Gómez M., Nicolás L., Rödel H.G., Bautista A. Possible contribution of position in the litter huddle to long-term differences in behavioral style in the domestic rabbit. Physiol. Behav. 2011, 104:778-785.
43. Rödel H.G., Bautista A., García-Torres E., Martínez-Gómez M., Hudson R. Why do heavy littermates grow better than lighter ones? A study in wild and domestic European rabbits. Physiol. Behav. 2008, 95:441-448.
44. Rödel H.G., Prager G., Stefanski V., von Holst D., Hudson R. Separating maternal and litter-size effects on early postnatal growth in two species of altricial small mammals. Physiol. Behav. 2008, 93:826-834.
45. Rödel H.G., Hudson R., von Holst D. Optimal litter size for individual growth of European rabbit pups depends on their thermal environment. Oecologia 2008, 155:677-689.
46. Rödel H.G., von Holst D., Kraus C. Family legacies: short- and long-term fitness consequences of early-life conditions in female European rabbits. J. Anim. Ecol. 2009, 78:789-797.
47. Rödel H.G., Starkloff A., Seltmann M.W., Prager G., von Holst D. Causes and predictors of nest mortality in a European rabbit population. Mamm. Biol. 2009, 74:198-209.
48. Rödel H.G., Dausmann K.H., Starkloff A., Schubert M., von Holst D., Hudson R. Diurnal nursing pattern of wild-type European rabbits under natural breeding conditions. Mamm. Biol. 2012, 77:441-446.
49. Satinoff E., McEwen G.N., Williams B.A. Behavioral fever in newborn rabbits. Science 1976, 193:1139-1140.
50. Seale P., Kajimura S., Yang W., Chin S., Rohas L.M., Uldry M., ve Tavernier G., Langin D., Spiegelman B.M. Transcriptional control of brown fat determination by PRDM16. Cell. Metab. 2007, 6:38-54.
51. Sharara-Chami R.I., Joachim M., Mulcahey M., Ebert S., Majzoub J.A. Effect of epinephrine deficiency on cold tolerance and on brown adipose tissue. Mol. Cell. Endocrinol. 2010, 328:34-39.
52. Sokal M., Sinclair J. Effect of temperature on growth of newborn rabbits. Biol. Neonate 1976, 28:1-11.
53. Sulloway J.F. Why siblings are like Darwin's finches. Birth order, parental investment, and adaptive divergence within the family. The Evolution of Personality and Individual Differences 2010, 86-119. Oxford University Press, Oxford. D.M. Buss, R.H. Hawley (Eds.).
54. Trillmich F., Hudson R. The emergence of personality in animals: the need for a developmental approach. Dev. Psychobiol. 2011, 53:505-509.
55. Vánai I., Farkas M., Donhoffer S.Z. Thermoregulatory heat production and the regulation of body temperature in the new-born rabbit. Acta Physiol. Acad. Sci. Hung. 1970, 38:299-315.
56. Vollmer R.R., Skott O. Rearing temperature and the sympathetic nervous system regulation of white and brown adipose tissue. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2002, 283:R1196-R1197.
57. Xiao X.Q., Williams S.M., Grayson B.E., Glavas M.M., Cowley M.A., Smith M.S., Grove K.L. Excess weight gain during the early postnatal period is associated with permanent reprogramming of brown adipose tissue adaptive thermogenesis. Endocrinology 2007, 148:4150-4159.
58. Zepeda Zempoaltecatl J.A. El peso relativo de los compañeros de camada y su efecto sobre el origen de las diferencias individuales durante el desarrollo temprano en el conejo doméstico 2015, Tesis de Maestría, Posgrado en Ciencias Biológicas, Universidad Autónoma de Tlaxcala, México.
59. Zepeda J.A., Reyes-Meza V., Martínez-Gómez M., Hudson R., Bautista A. Contribution of intra-litter interactions to the development of individual differences in rabbit pups. Dev. Psychobiol. 2013, 55:791.