Helicobacter suis Infection in Mouse Induced not Only Gastric, but Hepatic and Pulmonary MALT Lymphoma: Relation to Substance P

Page: [3039 - 3045] Pages: 7

  • * (Excluding Mailing and Handling)

Abstract

Background: The hepatic and pulmonary MALT lymphoma (mucosa-associated lymphoid tissue lymphoma) is clinically occasionally observed but its pathogenesis is unknown and thought to be important to establish the treatment strategy.

Objectives: The present study was designed to clarify the characteristics of these lymphomas and the effect of the Helicobacter eradication regimen and substance P antagonist.

Methods: After the long term infection of Helicobacter suis to the C57BL/6 mice stomach, the whole organ was surveyed pathologically. Histochemical characteristics of the lesion and the localization of bacteria were observed. In addition, the effect of the administration of antibiotics and a proton pump inhibitor or the substance P antagonist was investigated.

Results: We have detected the hepatic and pulmonary MALT lymphoma after the long term infection. In situ hybridization study revealed the positive reaction of Helicobacter suis in the hepatic and pulmonary MALT lymphoma. After the administration of antibiotics and a proton pump inhibitor, the bacterial number has significantly decreased and the tumor size in the fundus, liver and lung markedly reduced. Substance P immunoreactivity was clearly shown in the lymphoma cells in the liver and lung, and the spantide II administration induced the marked decrease in the size of tumors.

Conclusion: By our experiments using the long term infection of Helicobacter suis to the C57BL/6 mice, we have detected the liver and pulmonary MALT lymphoma. In situ hybridization study suggested the direct interaction of this bacterium to the etiology of these lesions. Substance P within the lymphoma cells was suggested to work on the maintenance of the extragastric MALT lymphoma.

Keywords: Hepatic MALT lymphoma, pulmonary MALT lymphoma, Helicobacter suis, substance P, hybridization study, extragastric.

[1]
Zinzani PL, Magagnoli M, Ascani S, et al. Nongastrointestinal mucosa-associated lymphoid tissue (MALT) lymphomas: clinical and therapeutic features of 24 localized patients. Ann Oncol 1997; 8(9): 883-6.
[http://dx.doi.org/10.1023/A:1008278725106] [PMID: 9358939]
[2]
Wotherspoon AC, Ortiz-Hidalgo C, Falzon MR, Isaacson PG. Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma. Lancet 1991; 338(8776): 1175-6.
[http://dx.doi.org/10.1016/0140-6736(91)92035-Z] [PMID: 1682595]
[3]
Isaacson PG. Mucosa-associated lymphoid tissue lymphoma. Semin Hematol 1999; 36(2): 139-47.
[PMID: 10319382]
[4]
Yoneyama H, Matsuno K, Zhang Y, et al. Regulation by chemokines of circulating dendritic cell precursors, and the formation of portal tract-associated lymphoid tissue, in a granulomatous liver disease. J Exp Med 2001; 193(1): 35-49.
[http://dx.doi.org/10.1084/jem.193.1.35] [PMID: 11136819]
[5]
Nakamura M, Murayama SY, Serizawa H, et al. “Candidatus Helicobacter heilmannii” from a cynomolgus monkey induces gastric mucosa-associated lymphoid tissue lymphomas in C57BL/6 mice. Infect Immun 2007; 75(3): 1214-22.
[http://dx.doi.org/10.1128/IAI.01459-06] [PMID: 17194807]
[6]
Erin N, Duymuş O, Oztürk S, Demir N. Activation of vagus nerve by semapimod alters substance P levels and decreases breast cancer metastasis. Regul Pept 2012; 179(1-3): 101-8.
[http://dx.doi.org/10.1016/j.regpep.2012.08.001] [PMID: 22982142]
[7]
Lane DJ. 16S/23S rRNA sequencingE. Chichester, West Sussex, England: Stackebradt John Wiley and Sons 1991; pp. 115-75.
[8]
O’Rourke JL, Dixon MF, Jack A, Enno A, Lee A. Gastric B-cell mucosa-associated lymphoid tissue (MALT) lymphoma in an animal model of ‘Helicobacter heilmannii’ infection. J Pathol 2004; 203(4): 896-903.
[http://dx.doi.org/10.1002/path.1593] [PMID: 15258991]
[9]
Altschul SF, Madden TL, Schäffer AA, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25(17): 3389-402.
[http://dx.doi.org/10.1093/nar/25.17.3389] [PMID: 9254694]
[10]
Chisholm SA, Owen RJ. Development and application of a novel screening PCR assay for direct detection of ‘Helicobacter heilmannii’-like organisms in human gastric biopsies in Southeast England. Diagn Microbiol Infect Dis 2003; 46(1): 1-7.
[http://dx.doi.org/10.1016/S0732-8893(02)00547-3] [PMID: 12742311]
[11]
Tomb JF, White O, Kerlavage AR, et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 1997; 388(6642): 539-47.
[http://dx.doi.org/10.1038/41483] [PMID: 9252185]
[12]
O’Rourke JL, Solnick JV, Neilan BA, et al. Description of ‘Candidatus Helicobacter heilmannii’ based on DNA sequence analysis of 16S rRNA and urease genes. Int J Syst Evol Microbiol 2004; 54(Pt. 6): 2203-11.
[http://dx.doi.org/10.1099/ijs.0.63117-0] [PMID: 15545459]
[13]
Stefanini M, De Martino C, Zamboni L. Fixation of ejaculated spermatozoa for electron microscopy. Nature 1967; 216(5111): 173-4.
[http://dx.doi.org/10.1038/216173a0] [PMID: 4862079]
[14]
Wang JY, Montone KT. A rapid simple in situ hybridization method for herpes simplex virus employing a synthetic biotin-labeled oligonucleotide probe: a comparison with immunohistochemical methods for HSV detection. J Clin Lab Anal 1994; 8(2): 105-15.
[http://dx.doi.org/10.1002/jcla.1860080209] [PMID: 8189321]
[15]
Trebesius K, Adler K, Vieth M, Stolte M, Haas R. Specific detection and prevalence of Helicobacter heilmannii-like organisms in the human gastric mucosa by fluorescent in situ hybridization and partial 16S ribosomal DNA sequencing. J Clin Microbiol 2001; 39(4): 1510-6.
[http://dx.doi.org/10.1128/JCM.39.4.1510-1516.2001] [PMID: 11283079]
[16]
Matsui H, Aikawa C, Sekiya Y, Takahashi S, Murayama SY, Nakamura M. Evaluation of antibiotic therapy for eradication of “Candidatus Helicobacter heilmannii”. Antimicrob Agents Chemother 2008; 52(8): 2988-9.
[http://dx.doi.org/10.1128/AAC.01662-07] [PMID: 18490502]
[17]
Stalke P, Al-Soud WA, Bielawski KP, et al. Detection of Helicobacter species in liver and stomach tissues of patients with chronic liver diseases using polymerase chain reaction-denaturing gradient gel electrophoresis and immunohistochemistry. Scand J Gastroenterol 2005; 40(9): 1032-41.
[http://dx.doi.org/10.1080/00365520510023251] [PMID: 16165716]
[18]
Iida T, Iwahashi M, Nakamura M, et al. Primary hepatic low-grade B-cell lymphoma of MALT-type associated with Helicobacter pylori infection. Hepatogastroenterology 2007; 54(78): 1898-901.
[PMID: 18019744]
[19]
Wang X, Willén R, Andersson C, Wadström T. Development of high-grade lymphoma in Helicobacter pylori-infected C57BL/6 mice. APMIS 2000; 108(7-8): 503-8.
[http://dx.doi.org/10.1034/j.1600-0463.2000.d01-89.x] [PMID: 11167546]
[20]
Vermoote M, Vandekerckhove TTM, Flahou B, et al. Genome sequence of Helicobacter suis supports its role in gastric pathology. Vet Res (Faisalabad) 2011; 42: 51-9.
[http://dx.doi.org/10.1186/1297-9716-42-51] [PMID: 21414191]
[21]
Roussos A, Philippou N, Gourgoulianis KI. Helicobacter pylori infection and respiratory diseases: a review. World J Gastroenterol 2003; 9(1): 5-8.
[http://dx.doi.org/10.3748/wjg.v9.i1.5] [PMID: 12508341]
[22]
Yanai S, Nakai K, Tokuhara K, et al. A case of gastric MALT lymphoma discovered through pulmonary lesions. J Jpn Surg Assoc 2009; 70: 1970-4.
[http://dx.doi.org/10.3919/jjsa.70.1970]
[23]
Hennig IM, Laissue JA, Horisberger U, Reubi JC. Substance-P receptors in human primary neoplasms: tumoral and vascular localization. Int J Cancer 1995; 61(6): 786-92.
[http://dx.doi.org/10.1002/ijc.2910610608] [PMID: 7790112]
[24]
Kodama Y, Sasaki K, Murasato F, et al. MALT Lymphoma, stress ulcer and cholinergic nerves from the viewpoint of bilateral and unilateral truncal vagotomy and substance P. Curr Pharm Des 2018; 24(18): 1961-5.
[http://dx.doi.org/10.2174/1381612824666180516103027] [PMID: 29766790]
[25]
Ladizinski B, Bazakas A, Olsen EA. Aprepitant: a novel neurokinin-1 receptor/substance P antagonist as antipruritic therapy in cutaneous T-cell lymphoma. J Am Acad Dermatol 2012; 67(5): e198-9.
[http://dx.doi.org/10.1016/j.jaad.2012.02.008] [PMID: 23062910]