Keratinocyte growth factor supports pulmonary innate immune defense through maintenance of alveolar antimicrobial protein levels and macrophage function

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 310, Issue 9, 2016, Pages L868-L879

  Gardner, Jason C ^a   Wu, Huixing ^a   Noel, John G ^b   Ramser, Benjamin J ^a   Pitstick, Lori ^a   Saito, Atsushi ^a   Nikolaidis, Nikolaos M ^a   McCormack, Francis X ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b SHRINERS HOSPITALS FOR CHILDREN   (United States)

Author keywords

Alveolar macrophages; Collectins; Innate defense; Keratinocyte growth factor; Lysozyme; Pneumonia

Indexed keywords

ANTIMICROBIAL PROTEIN; BETA DEFENSIN 1; BETA DEFENSIN 3; BETA DEFENSIN 4; CALGRANULIN A; CALGRANULIN B; CATHELICIDIN; COLLECTIN; CXCL1 CHEMOKINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; INTERLEUKIN 6; KERATINOCYTE GROWTH FACTOR; LACTOFERRIN; LYSOZYME; PROTEIN; SECRETORY LEUKOCYTE PROTEINASE INHIBITOR; SHORT PLATE LUNG AND NASAL EPITHELIUM CLONE 1; SURFACTANT PROTEIN A; SURFACTANT PROTEIN D; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL CLEARANCE; CELL POPULATION; CONTROLLED STUDY; ESCHERICHIA COLI; FEMALE; GENE EXPRESSION; GRAM NEGATIVE INFECTION; IMMUNE DEFICIENCY; INNATE IMMUNITY; LUNG ALVEOLUS MACROPHAGE; LUNG INFECTION; LUNG LAVAGE; MACROPHAGE FUNCTION; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; TYPE 2 EPITHELIAL CELL; 129 MOUSE; ANIMAL; BACTERIAL PNEUMONIA; C57BL MOUSE; CELL CULTURE; ESCHERICHIA COLI INFECTION; GENETICS; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG ALVEOLUS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; COLLECTINS; ESCHERICHIA COLI INFECTIONS; FEMALE; FIBROBLAST GROWTH FACTOR 7; GENE EXPRESSION; HUMANS; IMMUNITY, INNATE; MACROPHAGES, ALVEOLAR; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MURAMIDASE; PNEUMONIA, BACTERIAL; PULMONARY ALVEOLI;

EID: 84983760971     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00363.2015     Document Type: Article

References (46)

1. Akinbi HT, Epaud R, Bhatt H, Weaver TE. Bacterial killing is enhanced by expression of lysozyme in the lungs of transgenic mice. J Immunol 165: 5760–5766, 2000.
2. Alpdogan O, Hubbard VM, Smith OM, Patel N, Lu S, Goldberg GL, Gray DH, Feinman J, Kochman AA, Eng JM, Suh D, Muriglan SJ, Boyd RL, van den Brink MR. Keratinocyte growth factor (KGF) is required for postnatal thymic regeneration. Blood 107: 2453–2460, 2006.
3. Boulos L, Prevost M, Barbeau B, Coallier J, Desjardins R. LIVE/ DEAD BacLight: application of a new rapid staining method for direct enumeration of viable and total bacteria in drinking water. J Microbiol Methods 37: 77–86, 1999.
4. Brauchle M, Angermeyer K, Hubner G, Werner S. Large induction of keratinocyte growth factor expression by serum growth factors and proinflammatory cytokines in cultured fibroblasts. Oncogene 9: 3199–3204, 1994.
5. Chedid M, Rubin JS, Csaky KG, Aaronson SA. Regulation of keratinocyte growth factor gene expression by interleukin 1. J Biol Chem 269: 10753–10757, 1994.
6. Chen Y, Chou K, Fuchs E, Havran WL, Boismenu R. Protection of the intestinal mucosa by intraepithelial γδ T cells. Proc Natl Acad Sci USA 99: 14338–14343, 2002.
7. De Moerlooze L, Spencer-Dene B, Revest JM, Hajihosseini M, Rosewell I, Dickson C. An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development 127: 483–492, 2000.
8. DeFrances CJ, Hall MJ. 2005 National Hospital Discharge Survey. Advance Data 1–19, 2007.
9. Deterding RR, Havill AM, Yano T, Middleton SC, Jacoby CR, Shannon JM, Simonet WS, Mason RJ. Prevention of bleomycin-induced lung injury in rats by keratinocyte growth factor. Proc Assoc Am Physicians 109: 254–268, 1997.
10. Erdag G, Medalie DA, Rakhorst H, Krueger GG, Morgan JR. FGF-7 expression enhances the performance of bioengineered skin. Mol Ther 10: 76–85, 2004.
11. Finch PW, Rubin JS. Keratinocyte growth factor/fibroblast growth factor 7, a homeostatic factor with therapeutic potential for epithelial protection and repair. Adv Cancer Res 91: 69–136, 2004.
12. Finch PW, Rubin JS, Miki T, Ron D, Aaronson SA. Human KGF is FGF-related with properties of a paracrine effector of epithelial cell growth. Science 245: 752–755, 1989.
13. Guo L, Degenstein L, Fuchs E. Keratinocyte growth factor is required for hair development but not for wound healing. Genes Dev 10: 165–175, 1996.
14. Hu XW, Zhang XP, Li BR, Zhang J, Wang Y. The protective effect of keratinocyte growth factor on lipopolysaccharide-induced acute lung injury in rat. Zhongguo Wei Zhong Bing Ji Jiu Yi Xue 22: 486–489, 2010.
15. Ibrahim HR, Thomas U, Pellegrini A. A helix-loop-helix peptide at the upper lip of the active site cleft of lysozyme confers potent antimicrobial activity with membrane permeabilization action. J Biol Chem 276: 43767– 43774, 2001.
16. Kishore U, Greenhough TJ, Waters P, Shrive AK, Ghai R, Kamran MF, Bernal AL, Reid KB, Madan T, Chakraborty T. Surfactant proteins SP-A and SP-D: structure, function and receptors. Mol Immunol 43: 1293–1315, 2006.
17. Kochanek KD, Murphy SL, Anderson RN, Scott C. Deaths: final data for 2002. Natl Vital Stat Rep 53: 1–115, 2004.
18. Kojicic M, Li G, Hanson AC, Lee KM, Thakur L, Vedre J, Ahmed A, Baddour LM, Ryu JH, Gajic O. Risk factors for the development of acute lung injury in patients with infectious pneumonia. Crit Care 16: R46, 2012.
19. Kollef MH, Sherman G, Ward S, Fraser VJ. Inadequate antimicrobial treatment of infections: a risk factor for hospital mortality among critically ill patients. Chest 115: 462–474, 1999.
20. Kuzmenko AI, Wu H, McCormack FX. Pulmonary collectins selectively permeabilize model bacterial membranes containing rough lipopolysaccharide. Biochemistry 45: 2679–2685, 2006.
21. Markart P, Faust N, Graf T, Na CL, Weaver TE, Akinbi HT. Comparison of the microbicidal and muramidase activities of mouse lysozyme M and P. Biochem J 380: 385–392, 2004.
22. Markart P, Korfhagen TR, Weaver TE, Akinbi HT. Mouse lysozyme M is important in pulmonary host defense against Klebsiella pneumoniae infection. Am J Respir Crit Care Med 169: 454–458, 2004.
23. McCormack FX, Gibbons R, Ward SR, Kuzmenko A, Wu H, Deepe GS Jr. Macrophage-independent fungicidal action of the pulmonary collectins. J Biol Chem 278: 36250–36256, 2003.
24. McCormack FX, Whitsett JA. The pulmonary collectins SP-A and SP-D orchestrate innate immunity in the lung. J Clin Invest 109: 707–712, 2002.
25. Panos RJ, Bak PM, Simonet WS, Rubin JS, Smith LJ. Intratracheal instillation of keratinocyte growth factor decreases hyperoxia-induced mortality in rats. J Clin Invest 96: 2026–2033, 1995.
26. Pasula R, Azad AK, Gardner JC, Schlesinger LS, McCormack FX. Keratinocyte growth factor administration attenuates murine pulmonary Mycobacterium tuberculosis infection through granulocyte-macrophage colony-stimulating factor (GM-CSF)-dependent macrophage activation and phagolysosome fusion. J Biol Chem 290: 7151–7159, 2015.
27. Peng C, Chen B, Kao HK, Murphy G, Orgill DP, Guo L. Lack of FGF-7 further delays cutaneous wound healing in diabetic mice. Plast Reconstr Surg 128: 673e–684e, 2011.
28. Peng C, He Q, Luo C. Lack of keratinocyte growth factor retards angiogenesis in cutaneous wounds. J Int Med Res 39: 416–423, 2011.
29. Qiao J, Uzzo R, Obara-Ishihara T, Degenstein L, Fuchs E, Herzlinger D. FGF-7 modulates ureteric bud growth and nephron number in the developing kidney. Development 126: 547–554, 1999.
30. Rubin J, Osada H, Finch P, Taylor W, Rudikoff S, Aaronson S. Purification and characterization of a newly identified growth factor specific for epithelial cells. Proc Natl Acad Sci USA 86: 802–806, 1989.
31. Sanale AR, Firth JD, Uitto VJ, Putnins EE. Keratinocyte growth factor (KGF)-1 and -2 protein and gene expression in human gingival fibroblasts. J Periodontal Res 37: 66–74, 2002.
32. Shyamsundar M, McAuley DF, Ingram RJ, Gibson DS, O’Kane D, McKeown ST, Edwards A, Taggart C, Elborn JS, Calfee CS, Matthay MA, O’Kane CM. Keratinocyte growth factor promotes epithelial survival and resolution in a human model of lung injury. Am J Respir Crit Care Med 189: 1520–1529, 2014.
33. Singh PK, Tack BF, McCray PB Jr, Welsh MJ. Synergistic and additive killing by antimicrobial factors found in human airway surface liquid. Am J Physiol Lung Cell Mol Physiol 279: L799–L805, 2000.
34. Spielberger R, Stiff P, Bensinger W, Gentile T, Weisdorf D, Kewalramani T, Shea T, Yanovich S, Hansen K, Noga S, McCarty J, LeMaistre CF, Sung EC, Blazar BR, Elhardt D, Chen MG, Emmanouilides C. Palifermin for oral mucositis after intensive therapy for hematologic cancers. N Engl J Med 351: 2590–2598, 2004.
35. Takase HM, Itoh T, Ino S, Wang T, Koji T, Akira S, Takikawa Y, Miyajima A. FGF7 is a functional niche signal required for stimulation of adult liver progenitor cells that support liver regeneration. Genes Dev 27: 169–181, 2013.
36. Takeoka M, Ward WF, Pollack H, Kamp DW, Panos RJ. KGF facilitates repair of radiation-induced DNA damage in alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 272: L1174–L1180, 1997.
37. Tash JA, David SG, Vaughan EE, Herzlinger DA. Fibroblast growth factor-7 regulates stratification of the bladder urothelium. J Urol 166: 2536–2541, 2001.
38. Terauchi A, Johnson-Venkatesh EM, Toth AB, Javed D, Sutton MA, Umemori H. Distinct FGFs promote differentiation of excitatory and inhibitory synapses. Nature 465: 783–787, 2010.
39. Viget NB, Guery BP, Ader F, Neviere R, Alfandari S, Creuzy C, Roussel-Delvallez M, Foucher C, Mason CM, Beaucaire G, Pittet JF. Keratinocyte growth factor protects against Pseudomonas aeruginosa-induced lung injury. Am J Physiol Lung Cell Mol Physiol 279: L1199–L1209, 2000.
40. Welsh DA, Summer WR, Dobard EP, Nelson S, Mason CM. Keratinocyte growth factor prevents ventilator-induced lung injury in an ex vivo rat model. Am J Respir Crit Care Med 162: 1081–1086, 2000.
41. Whitsett JA. Intrinsic and innate defenses in the lung: intersection of pathways regulating lung morphogenesis, host defense, and repair. J Clin Invest 109: 565–569, 2002.
42. Wu H, Kuzmenko A, Wan S, Schaffer L, Weiss A, Fisher JH, Kim KS, McCormack FX. Surfactant proteins A and D inhibit the growth of Gram-negative bacteria by increasing membrane permeability. J Clin Invest 111: 1589–1602, 2003.
43. Wu H, Suzuki T, Carey B, Trapnell BC, McCormack FX. Keratinocyte growth factor augments pulmonary innate immunity through epitheliumdriven, GM-CSF-dependent paracrine activation of alveolar macrophages. J Biol Chem 286: 14932–14940, 2011.
44. Yano T, Deterding RR, Simonet WS, Shannon JM, Mason RJ. Keratinocyte growth factor reduces lung damage due to acid instillation in rats. Am J Respir Cell Mol Biol 15: 433–442, 1996.
45. Yano T, Mason RJ, Pan T, Deterding RR, Nielsen LD, Shannon JM. KGF regulates pulmonary epithelial proliferation and surfactant protein gene expression in adult rat lung. Am J Physiol Lung Cell Mol Physiol 279: L1146–L1158, 2000.
46. Yi ES, Williams ST, Lee H, Malicki DM, Chin EM, Yin S, Tarpley J, Ulich TR. Keratinocyte growth factor ameliorates radiation- and bleomycin-induced lung injury and mortality. Am J Pathol 149: 1963–1970, 1996.