Cellular expression of murine Ym1 and Ym2, chitinase family proteins, as revealed by in situ hybridization and immunohistochemistry (original) (raw)

Abstract

Ym is one of the chitinase family proteins, which are widely distributed in mammalian bodies and can bind glycosaminoglycans such as heparin/heparan sulfate. Ym1 is a macrophage protein produced in parasitic infections, while its isoform, Ym2, is upregulated in lung under allergic conditions. In the present study, we revealed the distinct cellular expression of Ym1 and Ym2 in normal mice by in situ hybridization and immunohistochemistry. Ym1 was principally expressed in the lung, spleen, and bone marrow, while Ym2 was found in the stomach. Ym1-expressing cells in the lung were alveolar macrophages, and the immunoreactivity for Ym1 was localized in rough endoplasmic reticulum. In the spleen, Ym1-expressing cells gathered in the red pulp and were electron microscopically identified as immature neutrophils. In the bone marrow, immature neutrophils were intensely immunoreactive, but lost this immunoreactivity with maturation. Moreover, needle-shaped crystals in the cytoplasm of macrophages, which formed erythroblastic islands, also showed intense Ym1 immunoreactivity. Ym2 expression was restricted to the stratified squamous epithelium in the junctional region between forestomach and glandular stomach. The function of Ym1 and Ym2 is still unclear; however, the distinct cellular localization under normal conditions suggests their important roles in hematopoiesis, tissue remodeling, or immune responses as an endogenous lectin.

Access this article

Log in via an institution

Subscribe and save

• Get 10 units per month
• Download Article/Chapter or eBook
• 1 Unit = 1 Article or 1 Chapter
• Cancel anytime Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

• Boot RG, Blommaart EF, Swart E, Ghauharali-van der Vlugt K, Bijl N, Moe C, Place A, Aerts JM (2001) Identification of a novel acidic mammalian chitinase distinct from chitotriosidase. J Biol Chem 276:6770–6778
  Article CAS PubMed Google Scholar
• Chang NCA, Hung SI, Hwa KY, Kato I, Chen JE, Liu CH, Chang AC (2001) A macrophage protein, Ym1, transiently expressed during inflammation is a novel mammalian lectin. J Biol Chem 276:17497–17506
  Article CAS PubMed Google Scholar
• Feldmesser M, Kress Y, Casadevall A (2001) Intracellular crystal formation as a mechanism of cytotoxicity in murine pulmonary Cryptococcus neoformans infection. Infect Immun 69:2723–2727
  Article PubMed Google Scholar
• Green EU (1942) On the occurrence of crystalline material in the lungs of normal and cancerous Swiss mice. Cancer Res 2:210–217
  CAS Google Scholar
• Guo L, Johnson RS, Schuh JCL (2000) Biochemical characterization of endogenously formed eosinophilic crystals in the lungs of mice. J Biol Chem 275:8032–8037
  Article CAS PubMed Google Scholar
• Hakala BE, White C, Recklies AD (1993) Human cartilage gp-39, a major secretory product of articular chondrocytes and synovial cells, is a mammalian member of a chitinase protein family. J Biol Chem 268:25803–25810
  CAS PubMed Google Scholar
• Harbord M, Novelli M, Canas B, Power D, Davis C, Godovac-Zimmermann J, Roes J, Segal AW (2002) Ym1 is a neutrophil granule protein that crystallizes in p47_phox_-deficient mice. J Biol Chem 277:5468–5475
  Article CAS PubMed Google Scholar
• Henrissat B (1999) Classification of chitinase modules. In: Jolle SP, Muzzarelli RAA (eds) Chitin and chitinases. Birkhauser, Basel, pp 137–156
• Henrissat B, Bairoch A (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 293:781–788
  CAS PubMed Google Scholar
• Hu B, Trinh K, Figueira WF, Price PA (1996) Isolation and sequence of a novel human chondrocyte protein related to mammalian members of the chitinase protein family. J Biol Chem 271:19415–19420
  Article CAS PubMed Google Scholar
• Huffnagle GB, Boyd MB, Street NE, Lipscomb MF (1998) IL-5 is required for eosinophil recruitment, crystal deposition, and mononuclear cell recruitment during a pulmonary Cryptococcus neoformans infection in genetically susceptible mice (C57BL/6). J Immunol 160:2393–2400
  CAS PubMed Google Scholar
• Hung SI, Chang AC, Kato I, Chang NCA (2002) Transient expression of Ym1, a heparin-binding lectin, during developmental hematopoiesis and inflammation. J Leukoc Biol 72:72–82
  CAS PubMed Google Scholar
• Jin HM, Copeland NG, Gilbert DJ, Jenkins NA, Kirkpatrick RB, Rosenberg M (1998) Genetic characterization of the murine Ym1 gene and identification of a cluster of highly homologous genes. Genomics 54:316–322
  Article CAS PubMed Google Scholar
• Kirkpatrick RB, Emery JG, Connor JR, Dodds R, Lysko PG, Rosenverg M (1997) Induction and expression of human cartilage glycoprotein 39 in rheumatoid inflammatory and peripheral blood monocyte-derived macrophages. Exp Cell Res 237:46–54
  Article CAS PubMed Google Scholar
• Kuby J (1997) Cells and organs of the immune system. In: Kuby J (ed) Immunology, 3rd edn. Freeman, New York, pp 47–83
• Leenen PJ, Melis M, Slieker WA, Van Ewijk W (1990) Murine macrophage precursor characterization. II. Monoclonal antibodies against macrophage precursor antigens. Eur J Immunol 20:27–34
  CAS PubMed Google Scholar
• Malette B, Paquette Y, Merlen Y, Bleau G (1995) Oviductins possess chitinase- and mucin-like domains: a lead in the search for the biological function of these oviduct-specific ZP-associating glycoproteins. Mol Reprod Dev 41:384–397
  CAS PubMed Google Scholar
• Morrison BW, Leder P (1994) neu and ras initiate murine mammary tumors that share genetic markers generally absent in c-myc and _int_-2-initiated tumors. Oncogene 9:3417–3426
  CAS PubMed Google Scholar
• Mowa CN, Iwanaga T (2000) Differential distribution of estrogen receptor α and β mRNAs in the female reproductive organ of rats as revealed by in situ hybridization. J Endocrinol 165:59–66
  CAS PubMed Google Scholar
• Murray AB, Luz A (1990) Acidophilic macrophage pneumonia in laboratory mice. Vet Pathol 27:274–281
  CAS PubMed Google Scholar
• Nyirkos P, Golds EE (1990) Human synovial cells secrete a 39 kDa protein similar to a bovine mammary protein expressed during the non-lactating period. Biochem J 269:265–268
  CAS PubMed Google Scholar
• Owhashi M, Arita H, Hayai N (2000) Identification of a novel eosinophil chemotactic cytokine (ECF-L) as a chitinase family protein. J Biol Chem 275:1279–1286
  Article CAS PubMed Google Scholar
• Renkema GH, Boot RG, Muijsers AO, Donker-Koopman WE, Aerts JM (1995) Purification and characterization of human chitotriosidase, a novel member of the chitinase family of proteins. J Biol Chem 270:2198–2202
  Article CAS PubMed Google Scholar
• Schuh JACL, Morrissey PJ, Fanslow WC, Pettit DK (1997) Eosinophilic crystals at sites of inflammation in the lung and subcutis of mice. Vet Pathol 34:493
  Google Scholar
• Sendai Y, Komiya H, Suzuki K, Onuma T, Kikuchi M, Hoshi H, Araki Y (1995) Molecular cloning and characterization of a mouse oviduct-specific glycoprotein. Biol Reprod 53:285–294
  CAS PubMed Google Scholar
• Shackelton LM, Mann DM, Millis AJT (1995) Identification of a 38-kDa heparin-binding glycoprotein (gp38 k) in differentiating vascular smooth muscle cells as a member of a group of proteins associated with tissue remodeling. J Biol Chem 270:13076–13083
  Article CAS PubMed Google Scholar
• Towbin H, Gordon J (1984) Immunoblotting and dot immunobinding: current status and outlook. J Immunol Methods 72:313–340
  CAS PubMed Google Scholar
• Ward JM (1978) Pulmonary pathology of the motheaten mouse. Vet Pathol 15:170–178
  CAS PubMed Google Scholar
• Ward JM, Yoon M, Anver MR, Haines DC, Kudo G, Gonzalez FJ, Kimura S (2001) Hyalinosis and Ym1/Ym2 gene expression in the stomach and respiratory tract of 129S4/SvJae and wild-type and CYP1A2-null B6, 129 mice. Am J Pathol 158:323–332
  CAS PubMed Google Scholar
• Webb DC, McKenzie ANJ, Foster PS (2001) Expression of the Ym2 lectin-binding protein is dependent on interleukin (IL)-4 and IL-13 signal transduction. J Biol Chem 276:41969–41976
  Article CAS PubMed Google Scholar
• Zhu A, Homer RJ, Wang Z, Chen Q, Geba GP, Wang J, Zhang Y, Elias JA (1999) Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J Clin Invest 103:779–788
  CAS PubMed Google Scholar

Download references

Acknowledgements

This work was supported by a grant from the Ministry of Education, Science, Sport, and Culture, Japan (number 15390052 to T.I.). The authors thank Prof. Hiroshi Kitagawa, Kobe University, for his kind advice.

Author information

Authors and Affiliations

1. Laboratory of Cytology and Histology, Graduate School of Medicine, Hokkaido University, Kita 15-Nishi 7, Kita-ku, 060-8638, Sapporo, Japan
   Wakako Fujimoto & Toshihiko Iwanaga
2. Laboratory of Anatomy, Graduate School of Veterinary Medicine, Hokkaido University, Kita 18-Nishi 9, Kita-ku, 060-0818, Sapporo, Japan
   Junko Nio, Akihiro Konno & Yasuhiro Kon
3. Faculty of Integrated Arts and Science, Tokushima University, 770-8502, Tokushima, Japan
   Makoto Owhashi

Authors

1. Junko Nio
   You can also search for this author inPubMed Google Scholar
2. Wakako Fujimoto
   You can also search for this author inPubMed Google Scholar
3. Akihiro Konno
   You can also search for this author inPubMed Google Scholar
4. Yasuhiro Kon
   You can also search for this author inPubMed Google Scholar
5. Makoto Owhashi
   You can also search for this author inPubMed Google Scholar
6. Toshihiko Iwanaga
   You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence toToshihiko Iwanaga.

Rights and permissions

About this article

Cite this article

Nio, J., Fujimoto, W., Konno, A. et al. Cellular expression of murine Ym1 and Ym2, chitinase family proteins, as revealed by in situ hybridization and immunohistochemistry.Histochem Cell Biol 121, 473–482 (2004). https://doi.org/10.1007/s00418-004-0654-4

Download citation

• Accepted: 22 April 2004
• Published: 18 May 2004
• Issue Date: June 2004
• DOI: https://doi.org/10.1007/s00418-004-0654-4

Keywords