Expression of the antimicrobial peptide cathelicidin in myeloid cells is required for lung tumor growth

Oncogene

Volumn 33, Issue 21, 2014, Pages 2709-2716

  Li, D ^a   Beisswenger, C ^a   Herr, C ^a   Schmid, R M ^b   Gallo, R L ^c   Han, G ^a   Zakharkina, T ^a   Bals, R ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

antimicrobial peptide; cathelicidin; inflammation; Lung cancer; macrophage

Indexed keywords

CARISOPRODOL; CATHELICIDIN; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CATHELICIDIN RELATED ANTIMICROBIAL PEPTIDE; CIGARETTE SMOKE; POLYPEPTIDE ANTIBIOTIC AGENT; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATORY CELL; LEWIS CARCINOMA; LUNG ALVEOLUS MACROPHAGE; LUNG TUMOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SURVIVAL TIME; TUMOR GROWTH; WILD TYPE;

ANIMALIA; BACTERIA (MICROORGANISMS); MUS;

ANIMALS; CARCINOMA, LEWIS LUNG; CATHELICIDINS; CELL LINE, TUMOR; COCULTURE TECHNIQUES; HUMANS; LUNG NEOPLASMS; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID CELLS; NEOPLASM TRANSPLANTATION; SMOKING; TRANSCRIPTION FACTOR RELA; TUMOR BURDEN;

EID: 84901506299     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.248     Document Type: Article

References (54)

1. Goldstraw P Ball D Jett JR Le Chevalier T Lim E Nicholson AG et al. Non-small-cell lung cancer. Lancet 2011; 378: 1727-1740.
2. Papi A Casoni G Caramo ri G Guzzinati I Boschetto P Ravenna F et al. COPD increases the risk of squamous histological subtype in smokers who develop non-small cell lung carcinoma. Thorax 2004; 59: 679-681. (Pubitemid 39061531)
3. Young RP Hopkins RJ Christmas T Black PN Metcalf P Gamble GD. COPD prevalence is increased in lung cancer independent of age sex and smoking history. Eur Respir J 2009; 34: 380-386.
4. Takahashi H Ogata H Nishigaki R Broide DH Karin M. Tobacco smoke promotes lung tumorigenesis by triggering IKKbeta-and JNK1-dependent inflammation. Cancer Cell 2010; 17: 89-97.
5. Grivennikov SI Karin M. Inflammation and oncogenesis: a vicious connection. Curr Opin Genet Dev 2010; 20: 65-71.
6. Coussens LM Werb Z. Inflammation and cancer Nature 2002 420860-867. (Pubitemid 36019639)
7. Bals R Wilson JM. Cathelicidins-A family of multifunctional antimicrobial peptides. Cell Mol Life Sci 2003; 60: 711-720. (Pubitemid 36570762)
8. Bals R Wang X Zasloff M Wilson JM. The peptide antibiotic LL-37/hCAP-18 is expressed in epithelia of the human lung where it has broad antimicrobial activity at the airway surface. Proc Natl Acad Sci USA 1998; 95: 9541-9546. (Pubitemid 28506267)
9. Gudmundsson GH Agerberth B Odeberg J Bergman T Olsson B Salcedo R. The human gene FALL39 and processing of the cathelin precursor to the antibacterial peptide LL-37 in granulocytes. Eur J Biochem 1996; 238: 325-332. (Pubitemid 26188246)
10. Frohm M Agerberth B Ahangari G Stahle-Backdahl M Liden S Wigzell H et al. The expression of the gene coding for the antibacterial peptide LL-37 is induced in human keratino cytes during inflammatory disorders. J Biol Chem 1997; 272: 15258-15263. (Pubitemid 27255544)
11. Gallo RL Kim KJ Bernfield M Kozak CA Zanetti M Merluzzi L et al. Identification of CRAMP a cathelin-r elated antimicrobial peptide expressed in the embryonic and adult mouse. J Biol Chem 1997; 272: 13088-13093. (Pubitemid 27216731)
12. Nizet V Ohtake T Lauth X Trowbridge J Rudisill J Dorschner RA et al. Innate antimicrobial peptide protects the skin from invasive bacterial infection. Nature 2001; 414: 454-457. (Pubitemid 34173727)
13. Bowdish DM Davidson DJ Hancock RE. A re-evaluation of the role of host defence peptides in mammalian immunity. Curr Protein Pept Sci 2005; 6: 35-51. (Pubitemid 40259800)
14. Bowdish DM Davidson DJ Scott MG Hancock RE. Immunomodulatory activities of small host defense peptides. Antimicrob Agents Chemother 2005; 49: 1727-1732. (Pubitemid 40631581)
15. Chromek M Slamova Z Bergman P Kovacs L Podracka L Ehren I et al. The antimicrobial peptide cathelicidin protects the urinary tract against invas ive bacterial infection. Nat Med 2006; 12: 636-641. (Pubitemid 43865231)
16. Kovach MA Ballinger MN Newstead MW Zeng X Bhan U Yu FS et al. Cathelicidin-related antimicrobial peptide is required for ef fective lung mucosal immunity in Gram-negative bacterial pneumonia. J Immunol 2012; 189: 304-311.
17. Koczulla R von Degenfeld G Kupatt C Krotz F Zahler S Gloe T et al. An ang iogenic role for the human peptide antibiotic LL-37/hCAP-18. J Clin Invest 2003; 111: 1665-1672. (Pubitemid 38057748)
18. Coffelt SB Waterman RS Florez L Honer zu Bentrup K Zwezdaryk KJ Tomchuck SL et al. Ovarian cancers overexpress the antimicrobial protein hCAP-and its derivative LL-37 increases ovarian cancer cell proliferation and invasion. Int J Cancer 2008; 122: 1030-1039. (Pubitemid 351214000)
19. Coffelt SB Marini FC Watson K Zwezdaryk KJ Dembinski JL LaMarca HL et al. The pro-inflammatory peptide LL-37 promotes ovarian tumor progression through recruitment of multipotent mesenchymal stromal cells. Proc Natl Acad Sci U SA 2009; 106: 3806-3811.
20. Heilborn JD Nilsson MF Jimenez CI Sandstedt B Borregaard N Tham E et al. Antimicrobial protein hCAP18/LL-37 is highly expressed in breast cancer and is a pu tative growth factor for epithelial cells. IntJ Cancer 2005; 114: 713-719. (Pubitemid 40344432)
21. Hensel JA Chanda D Kumar S Sawant A Grizzle WE Siegal GP et al. LL-37 as a therapeutic target for late stage prostate cancer. Prostate 2011; 71: 659-670.
22. von Haussen J Koczulla R Shaykhiev R Herr C Pinkenburg O Reimer D et al. The host defence peptide LL-37/hCAP-18 is a gro wth factor for lung cancer cells. Lung Cancer 2008; 59: 12-23.
23. Buchau AS Morizane S Trowbridge J Schauber J Kotol P Bui JD et al. The host defense peptide cathelicidin is requ ired for NK cell-mediated suppression of tumor growth. J Immunol 2010; 184: 369-378.
24. Kurosaka K Chen Q Yarovinsky F Oppenheim JJ Yang D. Mouse cathelin-related antimicrobial peptide c hemoattracts leukocytes using formyl peptide receptorlike 1/mouse formyl peptide receptor-like as the receptor and acts as an immune adjuvant. J Immunol 2005; 174: 6257-6265. (Pubitemid 40663818)
25. Yang D Chen Q Schmidt AP Anderson GM Wang JM Wooters J et al. LL-37 the neutrophil granule-and epithelial cell-derived cathelicidin utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils monocytes and T-cells. J Exp Med 2000; 192: 1069-1074.
26. Li G Domenico J Jia Y Lucas JJ Gelfand EW NF-kappaB-dependent induction of cathelicidin-related antimicrobial peptide in murine mast cells by lipopolysaccharide Int Arch Allergy Immunol 2009 150 122-132.
27. Li D Beisswenger C Herr C Hellberg J Han G Zakharkina T et al. Myeloid cell R elA/p65 promotes lung cancer proliferation through Wnt/b-catenin signaling in murine and human tumor cells. Oncogene 2014; 33: 1239-1248.
28. Tecle T Tripathi S Hartshorn KL. Review: defensins and cathelicidins in lung immunity. Innate Immun 2010; 16: 151-159.
29. Liu PT Stenger S Li H Wenzel L Tan BH Krutzik SR et al. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 2006; 311: 1770-1773.
30. Niyonsaba F Hirata M Ogawa H Nagaoka I. Epithelial cell-derived antibacterial peptides human beta-defensins and cathelicidin: multifunctional activities on mast cells. Curr Drug Targets Inflamm Allergy 2003; 2: 224-231.
31. Tjabringa GS Aarbiou J Ninaber DK Drijfhout JW Sorensen OE Borregaard N et al. The antimicrobial peptide LL-37 activates innate immunity at the airway epithelial surface by tran sactivation of the epidermal growth factor receptor. J Immunol 2003; 171: 6690-6696. (Pubitemid 37532101)
32. Shaykhiev R Beisswenger C Kaendler K Senske J Puechner A Damm T et al. The human endogenou s antibiotic LL-37 stimulates airway epithelial cell proliferation and wound closure. Am J Physiol Lung Cell Mol Physiol 2005; 289: 842-848.
33. Scott MG Davidson DJ Gold MR Bowdish D Hancock R E. The human antimicrobial peptide LL-37 is a multifunctional modulator of innate immune responses. J Immunol 2002; 169: 3883-3891.
34. Mookherjee N Brown KL Bowdish DM Doria S Falsafi R Hokamp K et al. Modulation of the TLR-mediated inflammatory response by the endogenous human host defense peptide LL-37. J Immunol 2006; 176: 2455-2464. (Pubitemid 43201696)
35. Heilborn JD Nilsson MF Kratz G Weber G Sorensen O Borregaard N et al. The cathelicidin anti-microbial peptide LL-37 is involved in re-epithelialization of human skin wounds and is lacking in chronic ulcer epithelium. J Invest Dermatol 2003; 120: 379-389. (Pubitemid 36298423)
36. Okumura K Itoh A Isogai E Hirose K Hosokawa Y Abiko Y et al. C-terminal domain of human CAP18 antimicrobial peptide induces apoptosis in oral squamous cell carcinoma SAS-H1 cells. Cancer Lett 2004; 212: 185-194. (Pubitemid 38997974)
37. Steinstraesser L Ring A Bals R Steinau HU Langer S. The human host defense peptide LL37/hCAP accelerates angiogenesis in PEGT/PBT biopolymers. Ann Plast ic Surg 2006; 56: 93-98. (Pubitemid 43042282)
38. Murdoch C Muthana M Coffelt SB Lewis CE. The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer 2008; 8: 618-631.
39. Gombart AF Borregaard N Koeffler HP. Human cathelicidin antimicrobial peptide (CAMP) gene is a direct target of the vitamin D receptor and is strongly up-regulated in myeloid cells by 1,25-dihydroxyvitamin D3. FASEB J . 2005; 19: 1067-1077. (Pubitemid 40946432)
40. Weber G Heilborn JD Chamorro Jimenez CI Hammarsjo A Torma H Stahle M. Vitamin D induces the antimicrobial protein hCAP18 in human skin. J Invest Dermatol 2005; 124: 1080-1082. (Pubitemid 40629115)
41. Heilborn JD Weber G Gronberg A Dieterich C Stahle M. Topical treatment with the vitamin D analogue calcipotriol enhances the upregulation of the antimicrobial protein hC AP18/LL-37 during wounding in human skin in vivo. Exp Dermatol 2010; 19: 332-338.
42. Liu PT Modlin RL. Human macrophage host defense against Mycobacterium tuberculosis. Curr Opin Immunol 2008; 20: 371-376.
43. Wang TT Nestel FP Bourdeau V Nagai Y Wang Q Liao J et al. Cutting edge: 1 25-dihydroxyvitamin D3 is a direct inducer of antimicrobial pepti de gene expression. J Immunol 2004; 173: 2909-2912. (Pubitemid 39141992)
44. Hase K Eckmann L Leopard JD Varki N Kagnoff MF. Cell differentiation is a key determinant of cathelicidin LL-37/human cationic antim icrobial protein 18 expression by human colon epithelium. Infect Immunol 2002; 70: 953-963. (Pubitemid 34083859)
45. Muehleisen B Bikle DD Aguilera C Burton DW Sen GL Deftos LJ et al. PTH/PTHrP and vi tamin D control antimicrobial peptide expression and susceptibility to bacterial skin infection. Sci Transl Med 2012; 4: 135-166.
46. Erdag G Morgan JR. Interleukin-1alpha and interleukin-6 enhance the antibacterial properties of cultured composite keratinocyte grafts. Ann Surg 2002; 235: 113-124. (Pubitemid 34062407)
47. Sorensen OE Cowland JB Theilgaard-Monch K Liu L Ganz T Borregaard N. Wound healing and expression of antimicrobial peptides/polypeptides in human keratinocytes a consequence of common growth factors J Immunol 2003 170 5583-5589. (Pubitemid 36617848)
48. Pestonjamasp VK Huttner KH Gallo RL. Processing site and gene structure for the murine antimicrobial peptide CRAMP. Peptides 2001; 22: 1643-1650. (Pubitemid 32918243)
49. Barnes PJ. Chronic obstructive pulmonary disease. N Engl J Med 2000; 343: 269-280. (Pubitemid 30490396)
50. Golec M Reichel C Mackiewicz B Skorska C Curzytek K Lemieszek M et al. Cathelicidin LL-37 granzymes TGF-beta1 and cytokines levels in induced sputum from farmers with and without COPD. A nn Agric Environ Med 2009; 16: 289-297.
51. Hess C Herr C Beisswenger C Zakharkina T Schmid RM Bals R. Myeloid RelA regulates pulmonary host defense networks. Eur Respir J 2010; 35: 343-352.
52. Buettner M Meinken C Bastian M Bhat R Stossel E Faller G et al. Inverse correlation of maturity and antibacterial activity in human dendritic cells. J Immunol 2005; 174: 4203-4209. (Pubitemid 40396000)
53. Beisswenger C Kandler K Hess C Garn H Felgentreff K Wegmann M et al. Allergic airway inflammation inhibits pulmonary antibacterial host defense. J Immunol 2006; 177: 1833-1837. (Pubitemid 44092521)
54. Beisswenger C Platz J Seifart C Vogelmeier C Bals R. Exposure of differentiated airway epithelial cells to volatile smoke in vitro. Respiration 2004; 71: 402-409. (Pubitemid 39179178)