Spatiotemporal Expression of Three Secretoglobin Proteins, SCGB1A1, SCGB3A1, and SCGB3A2, in Mouse Airway Epithelia

Overview

Journal J Histochem Cytochem

Publisher Sage Publications

Specialty Biochemistry

Date 2019 Feb 16

PMID 30768367

Citations 17

Authors

Xu Naizhen

Taketomo Kido

Shigetoshi Yokoyama

R Ilona Linnoila

Shioko Kimura

Affiliations

Soon will be listed here.

Abstract

Secretoglobins (SCGBs) are cytokine-like small molecular weight secreted proteins with largely unknown biological functions. Three SCGB proteins, SCGB1A1, SCGB3A1, and SCGB3A2, are predominantly expressed in lung airways. To gain insight into the possible functional relationships among the SCGBs, their protein and mRNA expression patterns were examined in lungs during gestation and in adult mice, using Scgb3a1-null and Scgb3a2-null mice as negative controls, by immunohistochemistry and by qRT-PCR analysis, respectively. The three SCGBs exhibited unique spatiotemporal expression patterns during embryogenesis. The lack of Scgb3a1 or Scgb3a2 did not affect expression of the other Scgb genes as determined by mRNA measurements. Moreover, the lack of Scgb3a1 or Scgb3a2 did not affect development of the pulmonary neuroepithelial bodies during embryogenesis, while the lack of Scgb3a2 may have resulted in slightly fewer ciliated cells than in the wild-type. These results suggest that SCGB1A1, SCGB3A1, and SCGB3A2 each may possess its own unique biological function.

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References

Castro C, Yang Y, Zhang Z, Linnoila R . Attenuation of pulmonary neuroendocrine differentiation in mice lacking Clara cell secretory protein. Lab Invest. 2000; 80(10):1533-40. DOI: 10.1038/labinvest.3780163. View

Klug J, Beier H, Bernard A, Chilton B, Fleming T, Lehrer R . Uteroglobin/Clara cell 10-kDa family of proteins: nomenclature committee report. Ann N Y Acad Sci. 2001; 923:348-54. DOI: 10.1111/j.1749-6632.2000.tb05549.x. View

Ryerse J, Hoffmann J, Mahmoud S, Nagel B, deMello D . Immunolocalization of CC10 in Clara cells in mouse and human lung. Histochem Cell Biol. 2001; 115(4):325-32. DOI: 10.1007/s004180100251. View

Krop I, Sgroi D, Porter D, Lunetta K, LeVangie R, Seth P . HIN-1, a putative cytokine highly expressed in normal but not cancerous mammary epithelial cells. Proc Natl Acad Sci U S A. 2001; 98(17):9796-801. PMC: 55532. DOI: 10.1073/pnas.171138398. View

Niimi T, Popescu N, Zhou Y, Levitt R, Kimura S . UGRP1, a uteroglobin/Clara cell secretory protein-related protein, is a novel lung-enriched downstream target gene for the T/EBP/NKX2.1 homeodomain transcription factor. Mol Endocrinol. 2001; 15(11):2021-36. DOI: 10.1210/mend.15.11.0728. View

Watson T, Reynolds S, Mango G, Boe I, Lund J, Stripp B . Altered lung gene expression in CCSP-null mice suggests immunoregulatory roles for Clara cells. Am J Physiol Lung Cell Mol Physiol. 2001; 281(6):L1523-30. DOI: 10.1152/ajplung.2001.281.6.L1523. View

Reynolds S, Reynolds P, Pryhuber G, Finder J, Stripp B . Secretoglobins SCGB3A1 and SCGB3A2 define secretory cell subsets in mouse and human airways. Am J Respir Crit Care Med. 2002; 166(11):1498-509. DOI: 10.1164/rccm.200204-285OC. View

Niimi T, Copeland N, Gilbert D, Jenkins N, Srisodsai A, Zimonjic D . Cloning, expression, and chromosomal localization of the mouse gene (Scgb3a1, alias Ugrp2) that encodes a member of the novel uteroglobin-related protein gene family. Cytogenet Genome Res. 2002; 97(1-2):120-7. DOI: 10.1159/000064067. View

Hicks S, Vassallo J, Dieter M, Lewis C, Whiteley L, Fix A . Immunohistochemical analysis of Clara cell secretory protein expression in a transgenic model of mouse lung carcinogenesis. Toxicology. 2003; 187(2-3):217-28. DOI: 10.1016/s0300-483x(03)00060-x. View

10.

Yang Y, Zhang Z, Mukherjee A, Linnoila R . Increased susceptibility of mice lacking Clara cell 10-kDa protein to lung tumorigenesis by 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone, a potent carcinogen in cigarette smoke. J Biol Chem. 2004; 279(28):29336-40. DOI: 10.1074/jbc.C400162200. View

11.

Krop I, Player A, Tablante A, Taylor-Parker M, Lahti-Domenici J, Fukuoka J . Frequent HIN-1 promoter methylation and lack of expression in multiple human tumor types. Mol Cancer Res. 2004; 2(9):489-94. View

12.

Chiba Y, Kusakabe T, Kimura S . Decreased expression of uteroglobin-related protein 1 in inflamed mouse airways is mediated by IL-9. Am J Physiol Lung Cell Mol Physiol. 2004; 287(6):L1193-8. DOI: 10.1152/ajplung.00263.2004. View

13.

Chiba Y, Srisodsai A, Supavilai P, Kimura S . Interleukin-5 reduces the expression of uteroglobin-related protein (UGRP) 1 gene in allergic airway inflammation. Immunol Lett. 2005; 97(1):123-9. PMC: 1343456. DOI: 10.1016/j.imlet.2004.10.013. View

14.

Chiba Y, Kurotani R, Kusakabe T, Miura T, Link B, Misawa M . Uteroglobin-related protein 1 expression suppresses allergic airway inflammation in mice. Am J Respir Crit Care Med. 2006; 173(9):958-64. PMC: 2582904. DOI: 10.1164/rccm.200503-456OC. View

15.

Lee Y, Zhang Z, Mukherjee A . Mice lacking uteroglobin are highly susceptible to developing pulmonary fibrosis. FEBS Lett. 2006; 580(18):4515-20. DOI: 10.1016/j.febslet.2006.07.031. View

16.

Mukherjee A, Zhang Z, Chilton B . Uteroglobin: a steroid-inducible immunomodulatory protein that founded the Secretoglobin superfamily. Endocr Rev. 2007; 28(7):707-25. DOI: 10.1210/er.2007-0018. View

17.

Kurotani R, Tomita T, Yang Q, Carlson B, Chen C, Kimura S . Role of secretoglobin 3A2 in lung development. Am J Respir Crit Care Med. 2008; 178(4):389-98. PMC: 2542440. DOI: 10.1164/rccm.200707-1104OC. View

18.

Tomita T, Kido T, Kurotani R, Iemura S, Sterneck E, Natsume T . CAATT/enhancer-binding proteins alpha and delta interact with NKX2-1 to synergistically activate mouse secretoglobin 3A2 gene expression. J Biol Chem. 2008; 283(37):25617-25627. PMC: 2533088. DOI: 10.1074/jbc.M805140200. View

19.

Tachihara-Yoshikawa M, Ishida T, Watanabe K, Sugawara A, Kanazawa K, Kanno R . Expression of secretoglobin3A2 (SCGB3A2) in primary pulmonary carcinomas. Fukushima J Med Sci. 2009; 54(2):61-72. PMC: 2743607. DOI: 10.5387/fms.54.61. View

20.

Rock J, Onaitis M, Rawlins E, Lu Y, Clark C, Xue Y . Basal cells as stem cells of the mouse trachea and human airway epithelium. Proc Natl Acad Sci U S A. 2009; 106(31):12771-5. PMC: 2714281. DOI: 10.1073/pnas.0906850106. View