Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Transient treatment of pregnant Merino ewes with modulators of cortisol biosynthesis coinciding with primary wool follicle initiation alters lifetime wool growth

M. L. McDowall A D , N. S. Watson-Haigh B , N. M. Edwards A , H. N. Kadarmideen B , G. S. Nattrass C , H. A. McGrice A C and P. I. Hynd A
+ Author Affiliations
- Author Affiliations

A School of Animal and Veterinary Sciences, The University of Adelaide, Roseworthy Campus, Roseworthy, SA 5371, Australia.

B Systems Genetics, Commonwealth Scientific and Industrial Research Organisation Livestock Industries, James Cook University, Townsville, Qld 4814, Australia.

C South Australian Research and Development Institute Livestock and Farming Systems, JS Davies Building, Roseworthy Campus, Roseworthy, SA 5371, Australia.

D Corresponding author. Email: melanie.mcdowall@adelaide.edu.au

Animal Production Science 53(10) 1101-1111 https://doi.org/10.1071/AN12193
Submitted: 5 July 2012  Accepted: 31 December 2012   Published: 16 April 2013

Abstract

The economically important characteristics of the adult fleece of Merino sheep, such as increases in clean fleece weight, fibre length, fibre diameter and crimp characteristics are determined during critical phases of fetal development of the skin and its appendages. Genetics plays a major role in the development of traits, but the maternal uterine environment could also influence development. Treatment of pregnant ewes with cortisol and its analogues has previously been shown to produce changes in wool follicle morphology. The aim of this study was to determine the effect of transient manipulation of maternal cortisol status during critical phases of wool follicle initiation and development in utero. From Days 55–65 post-conception, singleton-bearing Merino ewes were treated with metyrapone (cortisol inhibitor) or betamethasone (cortisol analogue). Lambs exposed to metyrapone in utero were born with hairier birthcoats than the control or betamethasone treatment groups (P < 0.05), displayed a 10% increase in staple length and a reduction in crimp frequency for the first three shearings (P < 0.05). Co-expression network analysis of microarray data revealed up-regulation of members of the transforming growth factor-β and chemokine receptor superfamilies, gene families known to influence hair and skin development. These experiments demonstrate that presumptive transient manipulation of maternal cortisol status coinciding with the initiation of fetal wool follicle development results in long-term alteration in fleece characteristics, namely fibre length and fibre crimp frequency. These results indicate it is possible to alter the lifetime wool production of Merino sheep with therapeutics targeted to gene expression during key windows of development in utero.


References

Barker DJ, Eriksson JG, Forsen T, Osmond C (2002) Fetal origins of adult disease: strength of effects and biological basis. International Journal of Epidemiology 31, 1235–1239.
Fetal origins of adult disease: strength of effects and biological basis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s%2FosVOksw%3D%3D&md5=9be715c92cc41e4ebcf980979c983a35CAS | 12540728PubMed |

Brakebusch C, Grose R, Quondamatteo F, Ramirez A, Jorcano JL, Pirro A, Svensson M, Herken R, Sasaki T, Timpl R, Werner S, Fassler R (2000) Skin and hair follicle integrity is crucially dependent on beta 1 integrin expression on keratinocytes. The EMBO Journal 19, 3990–4003.
Skin and hair follicle integrity is crucially dependent on beta 1 integrin expression on keratinocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmsVKqurY%3D&md5=c10a3afd2329aae36cf037481207f303CAS | 10921880PubMed |

Brettschneider J, Collin F, Bolstad BM, Speed TP (2008) Quality assessment for short oligonucleotide microarray data. Technometrics 50, 241–264.
Quality assessment for short oligonucleotide microarray data.Crossref | GoogleScholarGoogle Scholar |

Carlson MRJ, Zhang B, Fang Z, Mischel PS, Horvath S, Nelsen SF (2006) Gene connectivity, function, and sequence conservation: predictions from modular yeast co-expression networks. BioMed Central Genomics 7, 40

Carter HB (1939) Fleece density and the histology of the Merino skin. Australian Veterinary Journal 15, 210–213.
Fleece density and the histology of the Merino skin.Crossref | GoogleScholarGoogle Scholar |

Carter HB, Clarke WH (1957) The hair follicle group and skin follicle population of Australian Merino sheep. Australian Journal of Agricultural Research 8, 91–108.
The hair follicle group and skin follicle population of Australian Merino sheep.Crossref | GoogleScholarGoogle Scholar |

Chuong CM (Ed.) (1998) ‘Basis of epithelial appendage morphogenesis.’ (Landes Bioscience: Austin, TX)

DeLemos RA, Shermeta DW, Knelson JH, Kotas R, Avery ME (1970) Acceleration of appearance of pulmonary surfactant in the fetal lamb by administration of corticosteroids. The American Review of Respiratory Disease 102, 459–461.

Démarchez M, Mauger A, Herbage D, Sengel P (1984) Effect of hydrocortisone on skin development in the chick embryo: ultrastructural, immunohistological, and biochemical analysis. Developmental Biology 106, 15–25.
Effect of hydrocortisone on skin development in the chick embryo: ultrastructural, immunohistological, and biochemical analysis.Crossref | GoogleScholarGoogle Scholar | 6386570PubMed |

Fisher CJ, O’Guin WM, Sawyer RH (1984) Altered keratin biosynthesis follows inhibition of scale morphogenesis by hydrocortisone. Developmental Biology 106, 45–52.
Altered keratin biosynthesis follows inhibition of scale morphogenesis by hydrocortisone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXjsVyj&md5=14d5a5a907deff4363f92b0b0eeee601CAS | 6208069PubMed |

Fuller TF, Ghazalpour A, Aten JE, Drake TA, Lusis AJ, Horvath S (2007) Weighted gene coexpression network analysis strategies applied to mouse weight. Mammalian Genome 18, 463–472.
Weighted gene coexpression network analysis strategies applied to mouse weight.Crossref | GoogleScholarGoogle Scholar | 17668265PubMed |

Gautier L, Cope L, Bolstad BM, Irizarry RA (2004) Affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20, 307–315.
Affy-analysis of Affymetrix GeneChip data at the probe level.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXht1Kksr4%3D&md5=2e82f858578dbd528adaee4e088ec2c3CAS | 14960456PubMed |

Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biology 5, R80
Bioconductor: open software development for computational biology and bioinformatics.Crossref | GoogleScholarGoogle Scholar | 15461798PubMed |

Ghazalpour A, Doss S, Zhang B, Wang S, Plaisier C, Castellanos R, Brozell A, Schadt EE, Drake TA, Lusis AJ, Horvath S (2006) Integrating genetic and network analysis to characterize genes related to mouse weight. Public Library of Science Genetics 2, e130

Hardy MH (1992) The secret life of the hair follicle. Trends in Genetics 8, 55–61.

Hardy MH, Lyne AG (1956) The pre-natal development of wool follicles in Merino sheep. Australian Journal of Biological Sciences 9, 423–443.

Hocking Edwards JE, Newnham J, Ikegami M, Polk D, Jobe A (1999) Beta-methasone increases sweat gland formation and suppresses fibre formation in fetal sheep. Experimental Dermatology 8, 349–350.

Hogan BL, Yingling JM (1998) Epithelial/mesenchymal interactions and branching morphogenesis of the lung. Current Opinion in Genetics & Development 8, 481–486.
Epithelial/mesenchymal interactions and branching morphogenesis of the lung.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlvFGgtr4%3D&md5=12a85f2b4496725bfc0a444f0d0768bcCAS |

Jackson N, Nay T, Turner HN, Newton TH (1975) Response to selection in Australian Merino sheep. VII. Phenotypic and genetic parameters for some wool follicle characteristics and their correlation with wool and body traits. Australian Journal of Agricultural Research 26, 937–957.
Response to selection in Australian Merino sheep. VII. Phenotypic and genetic parameters for some wool follicle characteristics and their correlation with wool and body traits.Crossref | GoogleScholarGoogle Scholar |

Kadarmideen HN, Watson-Haigh NS, Andronicos NM (2011) Systems biology of ovine intestinal parasite resistance: disease gene modules and biomarkers. Molecular BioSystems 7, 235–246.
Systems biology of ovine intestinal parasite resistance: disease gene modules and biomarkers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFChtrrM&md5=d4050bfdad0790059859de0f2d2c8b90CAS | 21072409PubMed |

MacLennan NK, Dong J, Aten JE, Horvath S, Rahib L, Ornelas L, Dipple KM, McCabe ERB (2009) Weighted gene co-expression network analysis identifies biomarkers in glycerol kinase deficient mice. Molecular Genetics and Metabolism 98, 203–214.
Weighted gene co-expression network analysis identifies biomarkers in glycerol kinase deficient mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptlWku7o%3D&md5=2505638518cada1c30d11b09c34fa6b4CAS | 19546021PubMed |

Menzies M, Stockwell S, Brownlee A, Cam G (2009) Gene expression profiles of BMP4, FGF10 and cognate inhibitors, in the skin of foetal Merino sheep, at the time of secondary follicle branching. Experimental Dermatology 18, 877–879.
Gene expression profiles of BMP4, FGF10 and cognate inhibitors, in the skin of foetal Merino sheep, at the time of secondary follicle branching.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlCgtb7K&md5=5b3b3d76c2494e3da1166344e403e8caCAS | 19469906PubMed |

Moore GP, Jackson N, Isaacs K, Brown G (1996) Development and density of wool follicles in Merino sheep selected for single fibre characteristics. Australian Journal of Agricultural Research 47, 1195–1201.
Development and density of wool follicles in Merino sheep selected for single fibre characteristics.Crossref | GoogleScholarGoogle Scholar |

Nay T, Johnson H (1967) Follicle curvature and crimp size in some selected Australian Merino groups. Australian Journal of Agricultural Economics 18, 833–840.
Follicle curvature and crimp size in some selected Australian Merino groups.Crossref | GoogleScholarGoogle Scholar |

Nixon AJ (1993) A method for determining the activity state of hair follicles. Biotechnic & Histochemistry 68, 316–325.
A method for determining the activity state of hair follicles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c7it1ansA%3D%3D&md5=0abb59c96b15a7eb79da1cc7611eee82CAS |

Paus R, Cotsarelis G (1999) The biology of hair follicles. The New England Journal of Medicine 341, 491–497.
The biology of hair follicles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1MzltlGjtA%3D%3D&md5=9c9472388bf36a01adb6e26214870a37CAS | 10441606PubMed |

Ponzoni RW, Grimson RJ, Jaensch KS, Smith DH, Hynd PI (1997) Birth coat: is it worth taking it into consideration in Merino sheep genetic improvement programs? International Journal of Sheep and Wool Science 45, 12–26.

Ravasz E, Somera AL, Mongru DA, Oltvai ZN, Barabasi AL (2002) Hierarchical organization of modularity in metabolic networks. Science 297, 1551–1555.
Hierarchical organization of modularity in metabolic networks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmslSjtLs%3D&md5=75193e5b09c8d619896031943578d92cCAS | 12202830PubMed |

Saris CGJ, Horvath S, van Vught PWJ, van Es MA, Blauw HM, Fuller TF, Langfelder P, DeYoung J, Wokke JHJ, Veldink JH, van den Berg LH, Ophoff RA (2009) Weighted gene co-expression network analysis of the peripheral blood from Amyotrophic Lateral Sclerosis patients. BioMed Central Genomics 10, 405

Schadt EE, Lum PY (2006) Reverse engineering gene networks to identify key drivers of complex disease phenotypes. Journal of Lipid Research 47, 2601–2613.
Reverse engineering gene networks to identify key drivers of complex disease phenotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlSit7bK&md5=491b34d4fb77e4b29b7a7dda13c2d6a5CAS | 17012750PubMed |

Smith BT, Sabry K (1983) Glucocorticoid-thyroid synergism in lung maturation: a mechanism involving epithelial-mesenchymal interaction. Proceedings of the National Academy of Sciences of the United States of America 80, 1951–1954.
Glucocorticoid-thyroid synergism in lung maturation: a mechanism involving epithelial-mesenchymal interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhsleru7s%3D&md5=aeaf5ff3d7c38fc98eaccc18582f14ddCAS | 6300882PubMed |

Smith JL, Purvis IW, Haigh MG (2005) Crimp frequency effects on processing performance of superfine wool when staple length is held constant. International Journal of Sheep and Wool Science 53, 1–20.

Toland Thompson AC, Hebart MC, Penno NM, Hynd PI (2007) Perinatal wool follicle attrition coincides with elevated perinatal circulating cortisol concentration in Merino sheep. Australian Journal of Agricultural Research 58, 748–752.
Perinatal wool follicle attrition coincides with elevated perinatal circulating cortisol concentration in Merino sheep.Crossref | GoogleScholarGoogle Scholar |

Waite KA, Eng C (2003) From developmental disorder to heritable cancer: it’s all in the BMP/TGF-â family. Nature Reviews. Genetics 4, 763–773.
From developmental disorder to heritable cancer: it’s all in the BMP/TGF-â family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot1aksLY%3D&md5=c3ee32e33f3f33a370055fc2bb737c44CAS | 14526373PubMed |

Warnes KE, McMillen IC, Robinson JS, Coulter CL (2004) Differential actions of metyrapone on the fetal pituitary-adrenal axis in the sheep fetus in late gestation. Biology of Reproduction 71, 620–628.
Differential actions of metyrapone on the fetal pituitary-adrenal axis in the sheep fetus in late gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFWgurc%3D&md5=80266406e65ab5e57cd111b147b63cc1CAS | 15265784PubMed |

Watts J, Merritt GC, Lunney HW, Bennett NW, Dennis JA (1981) Observations on fibre diameter variation of sheep in relation to fleece rot and body strike susceptibility. Australian Veterinary Journal 57, 372–376.

Wu Z, Irizarry RA, Gentleman R, Murillo FM, Spencer F (2004) A model-based background adjustment for oligonucleotide expression arrays. Journal of the American Statistical Association 99, 909

Zhang B, Horvath S (2005) A general framework for weighted gene co-expression network analysis. Statistical Applications in Genetics and Molecular Biology 4, 17
A general framework for weighted gene co-expression network analysis.Crossref | GoogleScholarGoogle Scholar |

Zheng Q, Wang XJ (2008) GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis. Nucleic Acid Research 36, W358–W363.
GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptlKktLk%3D&md5=4ca9770f0d77b63d2239336cdeccb77eCAS |