Vesículas extracelulares
Uma forma de comunicação intrafolicular
DOI:
https://doi.org/10.35172/rvz.2017.v24.339Palavras-chave:
oócito, células do cummulus, estresse térmicoResumo
A produção de leite de bovinos taurinos apresenta uma série de entraves em regiões tropicais
como o Brasil. Um desses entraves é o estresse térmico (ET), que acarreta uma perda
econômica importante para os produtores. A perda de capital se deve em grande parte à queda
na produção de leite e nas falhas reprodutivas associadas ao ET. Já foram demonstradas várias
alterações reprodutivas oriundas do ET. A nível celular, foi notada a comunicação entre
células foliculares, por meio de vesículas extracelulares (EVs). Foi observada a comunicação
entre células do cummuluse células da granulosa por meio de EVs. Sendo assim, esta revisão
tem por finalidade correlacionar as EVs produzidas no interior dos folículos com os efeitos do
ET sobre os oócitos bovinos.
Referências
1. Igono MO, Bjotvedt G, Sanford-Crane HT. Environmental profile and critical
temperature effects on milk production of Holstein cows in desert climate. Int J
Biometeorol. 1992;36(2):77-87.
2. Boni R, Perrone LL, Cecchini S. Heat stress affects reproductive performance of high
producing dairy cows bred in an area of southern Apennines. Livest Sci. 2014;160:172-
7.
3. Rhoads ML, Rhoads RP, VanBaale MJ, Collier RJ, Sanders SR, Weber WJ, et al.
Effects of heat stress and plane of nutrition on lactating Holstein cows: I. Production,
metabolism, and aspects of circulating somatotropin. J Dairy Sci [Internet].
2009;92(5):1986-97.
4. Wilson SJ, Marion RS, Spain JN, Spiers DE, Keisler DH, Lucy MC. Effects of
controlled heat stress on ovarian function of dairy cattle. 1. Lactating cows. J Dairy Sci.
1998;81(8):2124-31.
5. Sartori R, Sartor-Bergfelt R, Mertens SA, Guenther JN, Parrish JJ, Wiltbank MC.
Fertilization and early embryonic development in heifers and lactating cows in summer
and lactating and dry cows in winter. J Dairy Sci. 2002;85(11):2803-12.ISSN 0102-5716 ISSN Eletrônico 2178-3764 Veterinária e Zootecnia
Dalanezi FM, Franchi FF, Fontes PK, Castilho ACS, Ferreira JCP. Vesículas extracelulares: uma forma de
comunicação intrafolicular. Vet. e Zootec. 2017 mar.; 24(1): 60-69.
65
6. De Rensis F, Scaramuzzi RJ. Heat stress and seasonal effects on reproduction in the
dairy cow: a review. Theriogenology. 2003;60(6):1139-51.
7. Mathivanan S, Ji H, Simpson RJ. Exosomes : extracellular organelles important in
intercellular communication. J Proteomics. 2010;73(10):1907-20.
8. Caby M, Lankar D, Vincendeau-Scherrer C, Bonnerot C. Exosomal-like vesicles are
present in human blood plasma. Int Immunol. 2005;17(7):879-87.
9. Gonzalez-Begne M, Lu B, Han X, Hagen FK, Hand AR, Melvin JE, et al. Proteomic
analysis of human parotid gland exosomes by multidimensional protein identification
technology (MudPIT). J Proteome Res. 2009;8(3):1304-14.
10. Berckmans RJ, Sturk A, Van Tienen LM, Schaap MCL, Nieuwland R. Cell-derived
vesicles exposing coagulant tissue factor in saliva. Blood. 2011;117(11):3172-80.
11. Pisitkun T, Shen R, Knepper MA. Identification and proteomic profiling of exosomes
in human urine. Proc Natl Acad Sci U S A. 2004;101(36):13368-73.
12. da Silveira JC, Veeramachaneni DNR, Winger QA, Carnevale EM, Bouma GJ. Cellsecreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: A
possible new form of cell communication within the ovarian follicle. Biol Reprod.
2012;86(3):71.
13. Taylor DD, Gercel-taylor C. The origin, function, and diagnostic potential of RNA
within extracellular vesicles present in human biological fluids. Front Genet. 2013;4:1-
12.
14. Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ.
Membrane-derived microvesicles: important and underappreciated mediators of cell-tocell communication. Leukemia. 2006;20(9):1487-95.
15. Bernabucci U, Lacetera N, Baumgard LH, Rhoads RP, Ronchi B, Nardone A.
Metabolic and hormonal acclimation to heat stress in domesticated ruminants. Animal.
2010;4(07):1167-83.
16. Sang Q, Yao Z, Wang H, Feng R, Wang H, Zhao X, et al. Identification of MicroRNAs
in human follicular fluid: characterization of MicroRNAs that govern steroidogenesis
in vitro and are associated with polycystic ovary syndrome in vivo. J Clin Endocrinol
Metab. 2013;98(7):3068-79.
17. Silveira JC, Winger QA, Bouma GJ, Carnevale EM. Effects of age on follicular fluid
exosomal microRNAs and granulosa cell transforming growth factor-b signalling
during follicle development in the mare. Reprod Fertil Dev. 2015;27(6):897-905.
18. Camussi G, Deregibus MC, Bruno S, Cantaluppi V, Biancone L. Exosomes /
microvesicles as a mechanism of cell-to-cell communication. Kidney Int.
2010;78(9):838-48.
19. Majka M, Janowska-Wieczorek A, Ratajczak J, Ehrenman K, Pietrzkowski Z, Anna
Kowalska M, et al. Numerous growth factors, cytokines, and chemokines are secreted
by human CD34+ cells, myeloblasts, erythroblasts, and megakaryoblasts and regulate
normal hematopoiesis in an autocrine/paracrine manner. Blood. 2001;97(10):3075-85.
20. Rustom A, Saffrich R, Markovic I, Walther P, Gerdes H. Nanotubular highways for
intercellular organelle transport. Science. 2004;303(5660):1007-10.
21. Sherer NM, Mothes W. Cytonemes and Tunnelling nanotubules in cell-cell
comunication and viral pathogenesis. Trends Cell Biol. 2009;18(9):414-20.
22. De Broe ME, Wieme RJ, Logghe GN, Roels F. Spontaneous shedding of plasma
membrane fragments by human cells in vivo and in vitro. Clin Chim Acta.
1977;81(3):237-45.
23. Pan BT, Teng K, Wu C, Adam M, Johnstone RM. Electron microscopic evidence for
externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J
Cell Biol. 1985;101(3):942-8.
24. Théry C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of
exosomes from cell culture supernatants and biological fluids. Curr Protoc cell Biol.
2006;Chapter 3:Unit 3.22.
25. Raposo G. B lymphocytes secrete antigen-presenting vesicles. J Exp Med.
1996;183(3):1161-72.
26. Heijnen BHFG, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release
two types of membrane vesicles: microvesicles by surface shedding and exosomes
derived from exocytosis of multivesicular bodies and a-granules. Blood.
1999;94(11):3791-9.
27. Rozmyslowicz T, Majka M, Kijowski J, Murphy SL, Conover DO, Poncz M, et al.
Platelet and Megakaryocyte derived microparticles transfer CXCR4 receptor to
CXCR4-null cells and make them susceptible to infection by X4-HIV. AIDS.
2003;17(1):33-42.
28. Kalra H, Simpson RJ, Ji H, Aikawa E, Altevogt P, Askenase P, et al. Vesiclepedia: a
compendium for extracellular vesicles with continuous community annotation. PLoS
Biol. 2012;10(12):8-12.
29. Johnstone RM. Exosomes biological significance: a concise review. Blood Cells Mol
Dis. 2006;36(2):315-21.
30. Théry C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune
responses. Nat Rev Immunol. 2009;9(8):581-93.
31. De Maio A. Extracellular heat shock proteins, cellular export vesicles, and the Stress
Observation System: a form of communication during injury, infection, and cell
damage. It is never known how far a controversial finding will go! Dedicated to
Ferruccio Ritossa. Cell Stress Chaperones. 2011;16(3):235-49
32. Janowska-Wieczorek A, Majka M, Kijowski J, Baj-Krzyworzeka M, Reca R, Robert
Turner A, et al. Platelet-derived microparticles bind to hematopoietic stem/progenitor
cells and enhance their engraftment. Blood. 2001;98(10):3143-9.
33. Morel O, Toti F, Hugel B, Freyssinet J. Cellular microparticles: a disseminated storage
pool of bioactive vascular effectors. Curr Opin Hematol. 2004;11(3):156-64.
34. Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more.
Trends Cell Biol. 2009;19(2):43-51.
35. Sohel MMH, Hoelker M, Noferesti SS, Salilew-Wondim D, Tholen E, Looft C, et al.
Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid:
implications for bovine oocyte developmental competence. PLoS One. 2013;8(11).
36. Silveira JC, Andrade GM, Nogueira MFG, Meirelles F V, Perecin F. Involvement of
miRNAs and cell-secreted vesicles in mammalian ovarian antral follicle development.
Reprod Sci. 2015;22(12):1474-83.
37. Hung W-T, Christenson LK, McGinnis LK. Extracellular vesicles from bovine
follicular fluid support cumulus expansion. Biol Reprod. 2015;93(5):117.
38. Gwazdauskas FC, Thatcher WW, Wilcox CJ. Physiological, environmental, and
hormonal factors at insemination which may affect conception. J Dairy Sci.
1973;56(7):873-7.
39. Rocha DR, Salles MGF, Moura AN, Araújo A. Impacto do estresse térmico na
reprodução da fêmea bovina. Rev Bras Reprod Anim. 2012;36(1):18-24.
40. Pirkkala L, Nykänen P, Sistonen L. Roles of the heat shock transcription factors in
regulation of the heat shock response and beyond. FASEB J. 2001;15(7):1118-31.
41. Lee WC, Wen HC, Chang CP, Chen MY, Lin MT. Heat shock protein 72
overexpression protects against hyperthermia, circulatory shock, and cerebral ischemia
during heatstroke. J Appl Physiol. 2006;100(6):2073-82.
42. Collier RJ, Collier JL, Rhoads RP, Baumgard LH. Invited review: genes involved in
the bovine heat stress response. J Dairy Sci. 2008;91(2):445-54.
43. Sonna LA, Fujita J, Gaffin SL, Lilly CM. Effects of heat and cold stress on mammalian
gene expression. J Appl Physiol. 2002;92(4):1725-42.
44. Lanks KW. Modulators of the eukaryotic heat shock response. Exp Cell Res.
1986;165(1):1-10.
45. Wolfenson D, Thatcher WW, Badinga L, Savio JD, Meidan R, Lew BJ, et al. Effect of
heat stress on follicular development during the estrous cycle in lactating dairy cattle.
Biol Reprod. 1995;52(5):1106-13.
46. Roth Z, Meidan R, Braw-Tal R, Wolfenson D. Immediate and delayed effects of heat
stress on follicular development and its association with plasma FSH and inhibin
concentration in cows. J Reprod Fertil. 2000;120(1):83-90.
47. Shaham-Albalancy A, Folman Y, Kaim M, Rosenberg M, Wolfenson D. Delayed
effect of low progesterone concentrations on bovine uterine PGF2α secretion in the
subsequent oestrous cycle. Reproduction. 2001;122(4):643-8.
48. El-Tarabany MS, El-Tarabany AA. Impact of maternal heat stress at insemination on
the subsequent reproductive performance of Holstein, Brown Swiss, and their crosses.
Theriogenology. 2015;84(9):1523-9.
49. Roman-Ponce H, Thatcher WW, Wilcox CJ. Hormonal interrelationships and
physiological responses of lactating dairy cows to a shade management system in a
subtropical environment. Theriogenology. 1981;16(2):139-54.
50. Gauthier D. The influence of season and shade on oestrous behaviour, timing of
preovulatory LH surge and the pattern of progesterone secretion in FFPN and Creole
heifers in a tropical climate. Reprod Nutr Dev. 1986;26(3):767-75.
51. Madan ML, Johnson HD. Environmental heat effects on bovine luteinizing hormone. J
Dairy Sci. 1973;56(11):1420-3.
52. Wise ME, Armstrong DV, Huber JT, Hunter R, Wiersma F. Hormonal alterations in
the lactating dairy cow in response to thermal stress. J Dairy Sci. 1988;71(9):2480-5.
53. Gilad E, Meidan R, Berman A, Graber Y, Wolfenson D. Effect of heat stress on tonic
and GnRH-induced gonadotrophin secretion in relation to concentration of oestradiol in
plasma of cyclic cows. J Reprod Fertil. 1993;99(2):315-21.
54. Lee CN. Environmental stress effects on bovine reproduction. Vet Clin North Am Food
Anim Pract. 1993;9(2):263-73.
55. Torres-Júnior JRS, Pires MFA, Sá WF, Ferreira AM, Viana JHM, Camargo LSA, et al.
Effect of maternal heat-stress on follicular growth and oocyte competence in Bos
indicus cattle. Theriogenology. 2008;69(2):155-66.
56. Andreu-Vázquez C, López-Gatius F, García-Ispierto I, Maya-Soriano MJ, Hunter RHF,
López-Béjar M. Does heat stress provoke the loss of a continuous layer of cortical
granules beneath the plasma membrane during oocyte maturation? Zygote.
2010;18(04):293-9.
57. Putney DJ, Drost M, Thatcher WW. Embryonic development in superovulated dairy
cattle exposed to elevated ambient temperatures between Days 1 to 7 post
insemination. Theriogenology. 1988;30(2):195-209.
58. Roth Z, Meidan R, Wolfenson D. Delayed effect of heat stress on steroid production in
medium-sized and preovulatory bovine follicles. Reproduction. 2001;121(5):745-51.
59. Zeron Y, Ocheretny A, Kedar O, Borochov A, Sklan D, Arav A. Seasonal changes in
bovine fertility: Relation to developmental competence of oocytes, membrane
properties and fatty acid composition of follicles. Reproduction. 2001;121(3):447-54.
60. Gendelman M, Roth Z. Seasonal effect on germinal vesicle-stage bovine oocytes Is
further expressed by alterations in transcript levels in the developing embryos
associated with reduced developmental competence. Biol Reprod. 2012;86(1):1-9.
temperature effects on milk production of Holstein cows in desert climate. Int J
Biometeorol. 1992;36(2):77-87.
2. Boni R, Perrone LL, Cecchini S. Heat stress affects reproductive performance of high
producing dairy cows bred in an area of southern Apennines. Livest Sci. 2014;160:172-
7.
3. Rhoads ML, Rhoads RP, VanBaale MJ, Collier RJ, Sanders SR, Weber WJ, et al.
Effects of heat stress and plane of nutrition on lactating Holstein cows: I. Production,
metabolism, and aspects of circulating somatotropin. J Dairy Sci [Internet].
2009;92(5):1986-97.
4. Wilson SJ, Marion RS, Spain JN, Spiers DE, Keisler DH, Lucy MC. Effects of
controlled heat stress on ovarian function of dairy cattle. 1. Lactating cows. J Dairy Sci.
1998;81(8):2124-31.
5. Sartori R, Sartor-Bergfelt R, Mertens SA, Guenther JN, Parrish JJ, Wiltbank MC.
Fertilization and early embryonic development in heifers and lactating cows in summer
and lactating and dry cows in winter. J Dairy Sci. 2002;85(11):2803-12.ISSN 0102-5716 ISSN Eletrônico 2178-3764 Veterinária e Zootecnia
Dalanezi FM, Franchi FF, Fontes PK, Castilho ACS, Ferreira JCP. Vesículas extracelulares: uma forma de
comunicação intrafolicular. Vet. e Zootec. 2017 mar.; 24(1): 60-69.
65
6. De Rensis F, Scaramuzzi RJ. Heat stress and seasonal effects on reproduction in the
dairy cow: a review. Theriogenology. 2003;60(6):1139-51.
7. Mathivanan S, Ji H, Simpson RJ. Exosomes : extracellular organelles important in
intercellular communication. J Proteomics. 2010;73(10):1907-20.
8. Caby M, Lankar D, Vincendeau-Scherrer C, Bonnerot C. Exosomal-like vesicles are
present in human blood plasma. Int Immunol. 2005;17(7):879-87.
9. Gonzalez-Begne M, Lu B, Han X, Hagen FK, Hand AR, Melvin JE, et al. Proteomic
analysis of human parotid gland exosomes by multidimensional protein identification
technology (MudPIT). J Proteome Res. 2009;8(3):1304-14.
10. Berckmans RJ, Sturk A, Van Tienen LM, Schaap MCL, Nieuwland R. Cell-derived
vesicles exposing coagulant tissue factor in saliva. Blood. 2011;117(11):3172-80.
11. Pisitkun T, Shen R, Knepper MA. Identification and proteomic profiling of exosomes
in human urine. Proc Natl Acad Sci U S A. 2004;101(36):13368-73.
12. da Silveira JC, Veeramachaneni DNR, Winger QA, Carnevale EM, Bouma GJ. Cellsecreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: A
possible new form of cell communication within the ovarian follicle. Biol Reprod.
2012;86(3):71.
13. Taylor DD, Gercel-taylor C. The origin, function, and diagnostic potential of RNA
within extracellular vesicles present in human biological fluids. Front Genet. 2013;4:1-
12.
14. Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ.
Membrane-derived microvesicles: important and underappreciated mediators of cell-tocell communication. Leukemia. 2006;20(9):1487-95.
15. Bernabucci U, Lacetera N, Baumgard LH, Rhoads RP, Ronchi B, Nardone A.
Metabolic and hormonal acclimation to heat stress in domesticated ruminants. Animal.
2010;4(07):1167-83.
16. Sang Q, Yao Z, Wang H, Feng R, Wang H, Zhao X, et al. Identification of MicroRNAs
in human follicular fluid: characterization of MicroRNAs that govern steroidogenesis
in vitro and are associated with polycystic ovary syndrome in vivo. J Clin Endocrinol
Metab. 2013;98(7):3068-79.
17. Silveira JC, Winger QA, Bouma GJ, Carnevale EM. Effects of age on follicular fluid
exosomal microRNAs and granulosa cell transforming growth factor-b signalling
during follicle development in the mare. Reprod Fertil Dev. 2015;27(6):897-905.
18. Camussi G, Deregibus MC, Bruno S, Cantaluppi V, Biancone L. Exosomes /
microvesicles as a mechanism of cell-to-cell communication. Kidney Int.
2010;78(9):838-48.
19. Majka M, Janowska-Wieczorek A, Ratajczak J, Ehrenman K, Pietrzkowski Z, Anna
Kowalska M, et al. Numerous growth factors, cytokines, and chemokines are secreted
by human CD34+ cells, myeloblasts, erythroblasts, and megakaryoblasts and regulate
normal hematopoiesis in an autocrine/paracrine manner. Blood. 2001;97(10):3075-85.
20. Rustom A, Saffrich R, Markovic I, Walther P, Gerdes H. Nanotubular highways for
intercellular organelle transport. Science. 2004;303(5660):1007-10.
21. Sherer NM, Mothes W. Cytonemes and Tunnelling nanotubules in cell-cell
comunication and viral pathogenesis. Trends Cell Biol. 2009;18(9):414-20.
22. De Broe ME, Wieme RJ, Logghe GN, Roels F. Spontaneous shedding of plasma
membrane fragments by human cells in vivo and in vitro. Clin Chim Acta.
1977;81(3):237-45.
23. Pan BT, Teng K, Wu C, Adam M, Johnstone RM. Electron microscopic evidence for
externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J
Cell Biol. 1985;101(3):942-8.
24. Théry C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of
exosomes from cell culture supernatants and biological fluids. Curr Protoc cell Biol.
2006;Chapter 3:Unit 3.22.
25. Raposo G. B lymphocytes secrete antigen-presenting vesicles. J Exp Med.
1996;183(3):1161-72.
26. Heijnen BHFG, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release
two types of membrane vesicles: microvesicles by surface shedding and exosomes
derived from exocytosis of multivesicular bodies and a-granules. Blood.
1999;94(11):3791-9.
27. Rozmyslowicz T, Majka M, Kijowski J, Murphy SL, Conover DO, Poncz M, et al.
Platelet and Megakaryocyte derived microparticles transfer CXCR4 receptor to
CXCR4-null cells and make them susceptible to infection by X4-HIV. AIDS.
2003;17(1):33-42.
28. Kalra H, Simpson RJ, Ji H, Aikawa E, Altevogt P, Askenase P, et al. Vesiclepedia: a
compendium for extracellular vesicles with continuous community annotation. PLoS
Biol. 2012;10(12):8-12.
29. Johnstone RM. Exosomes biological significance: a concise review. Blood Cells Mol
Dis. 2006;36(2):315-21.
30. Théry C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune
responses. Nat Rev Immunol. 2009;9(8):581-93.
31. De Maio A. Extracellular heat shock proteins, cellular export vesicles, and the Stress
Observation System: a form of communication during injury, infection, and cell
damage. It is never known how far a controversial finding will go! Dedicated to
Ferruccio Ritossa. Cell Stress Chaperones. 2011;16(3):235-49
32. Janowska-Wieczorek A, Majka M, Kijowski J, Baj-Krzyworzeka M, Reca R, Robert
Turner A, et al. Platelet-derived microparticles bind to hematopoietic stem/progenitor
cells and enhance their engraftment. Blood. 2001;98(10):3143-9.
33. Morel O, Toti F, Hugel B, Freyssinet J. Cellular microparticles: a disseminated storage
pool of bioactive vascular effectors. Curr Opin Hematol. 2004;11(3):156-64.
34. Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more.
Trends Cell Biol. 2009;19(2):43-51.
35. Sohel MMH, Hoelker M, Noferesti SS, Salilew-Wondim D, Tholen E, Looft C, et al.
Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid:
implications for bovine oocyte developmental competence. PLoS One. 2013;8(11).
36. Silveira JC, Andrade GM, Nogueira MFG, Meirelles F V, Perecin F. Involvement of
miRNAs and cell-secreted vesicles in mammalian ovarian antral follicle development.
Reprod Sci. 2015;22(12):1474-83.
37. Hung W-T, Christenson LK, McGinnis LK. Extracellular vesicles from bovine
follicular fluid support cumulus expansion. Biol Reprod. 2015;93(5):117.
38. Gwazdauskas FC, Thatcher WW, Wilcox CJ. Physiological, environmental, and
hormonal factors at insemination which may affect conception. J Dairy Sci.
1973;56(7):873-7.
39. Rocha DR, Salles MGF, Moura AN, Araújo A. Impacto do estresse térmico na
reprodução da fêmea bovina. Rev Bras Reprod Anim. 2012;36(1):18-24.
40. Pirkkala L, Nykänen P, Sistonen L. Roles of the heat shock transcription factors in
regulation of the heat shock response and beyond. FASEB J. 2001;15(7):1118-31.
41. Lee WC, Wen HC, Chang CP, Chen MY, Lin MT. Heat shock protein 72
overexpression protects against hyperthermia, circulatory shock, and cerebral ischemia
during heatstroke. J Appl Physiol. 2006;100(6):2073-82.
42. Collier RJ, Collier JL, Rhoads RP, Baumgard LH. Invited review: genes involved in
the bovine heat stress response. J Dairy Sci. 2008;91(2):445-54.
43. Sonna LA, Fujita J, Gaffin SL, Lilly CM. Effects of heat and cold stress on mammalian
gene expression. J Appl Physiol. 2002;92(4):1725-42.
44. Lanks KW. Modulators of the eukaryotic heat shock response. Exp Cell Res.
1986;165(1):1-10.
45. Wolfenson D, Thatcher WW, Badinga L, Savio JD, Meidan R, Lew BJ, et al. Effect of
heat stress on follicular development during the estrous cycle in lactating dairy cattle.
Biol Reprod. 1995;52(5):1106-13.
46. Roth Z, Meidan R, Braw-Tal R, Wolfenson D. Immediate and delayed effects of heat
stress on follicular development and its association with plasma FSH and inhibin
concentration in cows. J Reprod Fertil. 2000;120(1):83-90.
47. Shaham-Albalancy A, Folman Y, Kaim M, Rosenberg M, Wolfenson D. Delayed
effect of low progesterone concentrations on bovine uterine PGF2α secretion in the
subsequent oestrous cycle. Reproduction. 2001;122(4):643-8.
48. El-Tarabany MS, El-Tarabany AA. Impact of maternal heat stress at insemination on
the subsequent reproductive performance of Holstein, Brown Swiss, and their crosses.
Theriogenology. 2015;84(9):1523-9.
49. Roman-Ponce H, Thatcher WW, Wilcox CJ. Hormonal interrelationships and
physiological responses of lactating dairy cows to a shade management system in a
subtropical environment. Theriogenology. 1981;16(2):139-54.
50. Gauthier D. The influence of season and shade on oestrous behaviour, timing of
preovulatory LH surge and the pattern of progesterone secretion in FFPN and Creole
heifers in a tropical climate. Reprod Nutr Dev. 1986;26(3):767-75.
51. Madan ML, Johnson HD. Environmental heat effects on bovine luteinizing hormone. J
Dairy Sci. 1973;56(11):1420-3.
52. Wise ME, Armstrong DV, Huber JT, Hunter R, Wiersma F. Hormonal alterations in
the lactating dairy cow in response to thermal stress. J Dairy Sci. 1988;71(9):2480-5.
53. Gilad E, Meidan R, Berman A, Graber Y, Wolfenson D. Effect of heat stress on tonic
and GnRH-induced gonadotrophin secretion in relation to concentration of oestradiol in
plasma of cyclic cows. J Reprod Fertil. 1993;99(2):315-21.
54. Lee CN. Environmental stress effects on bovine reproduction. Vet Clin North Am Food
Anim Pract. 1993;9(2):263-73.
55. Torres-Júnior JRS, Pires MFA, Sá WF, Ferreira AM, Viana JHM, Camargo LSA, et al.
Effect of maternal heat-stress on follicular growth and oocyte competence in Bos
indicus cattle. Theriogenology. 2008;69(2):155-66.
56. Andreu-Vázquez C, López-Gatius F, García-Ispierto I, Maya-Soriano MJ, Hunter RHF,
López-Béjar M. Does heat stress provoke the loss of a continuous layer of cortical
granules beneath the plasma membrane during oocyte maturation? Zygote.
2010;18(04):293-9.
57. Putney DJ, Drost M, Thatcher WW. Embryonic development in superovulated dairy
cattle exposed to elevated ambient temperatures between Days 1 to 7 post
insemination. Theriogenology. 1988;30(2):195-209.
58. Roth Z, Meidan R, Wolfenson D. Delayed effect of heat stress on steroid production in
medium-sized and preovulatory bovine follicles. Reproduction. 2001;121(5):745-51.
59. Zeron Y, Ocheretny A, Kedar O, Borochov A, Sklan D, Arav A. Seasonal changes in
bovine fertility: Relation to developmental competence of oocytes, membrane
properties and fatty acid composition of follicles. Reproduction. 2001;121(3):447-54.
60. Gendelman M, Roth Z. Seasonal effect on germinal vesicle-stage bovine oocytes Is
further expressed by alterations in transcript levels in the developing embryos
associated with reduced developmental competence. Biol Reprod. 2012;86(1):1-9.
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Morales Dalanezi F, Fagali Franchi F, Kubo Fontes P, César de Souza Castilho A, Pinheiro Ferreira JC. Vesículas extracelulares: Uma forma de comunicação intrafolicular. RVZ [Internet]. 31º de março de 2017 [citado 19º de abril de 2024];24(1):60-9. Disponível em: https://rvz.emnuvens.com.br/rvz/article/view/339
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Este obra está licenciado com uma Licença Creative Commons Atribuição-NãoComercial 4.0 Internacional.
