Summary
In Melbourne, Australia, grass pollen allergens, especially from ryegrass, are a major cause of allergic hayfever and asthma. This review outlines recent developments in our understanding of how grass pollen allergens find their way into the atmosphere and how they are transported in particulate form. Much of this work has relied on antibody technology in immunological and immunocytochemical investigations. The localisation of allergens in situ has proved difficult due to their water-soluble character. Recently, allergens have been localised in developing ryegrass pollen by dryfixation, rapid-freeze and freeze-substitution techniques. This involved anthers being substituted in a mixture of aldehydes, organic solvents, and 2,2-dimethoxypropane. Incubation in dimethylsulfoxide prior to embedding in LR Gold resin provided good infiltration with freeze-substituted material. Immunogold-labelled sections show that the major allergens, Lol p 1 and Lol p 5, are synthesised in the pollen cytoplasm from the early bicellular stage, soon after the first starch granules are formed. From the early tricellular stage, Lol p 5 moves into the starch granules where it remains until maturity. Lol p 1 is localised in the cytoplasm of mature pollen grains. The incidence of airborne grass pollen, as measured in pollen traps, correlates with hayfever symptoms. Forecasting models which rely on rainfall and temperature data have been produced for the grass pollen (daily and seasonal) counts in Melbourne. Research over the past six years has shed light on the causes of grass-pollen-induced asthma. Micronic particles in the atmosphere may be starch granules originating from pollen grains osmotically ruptured by rainwater. Ultrastructural and immunological characterisation of micronic particles collected from outdoor air filters confirm the presence of airborne starch granules. These are loaded with grass pollen allergens, occur in the atmosphere especially after rainfall, and correlate significantly with instances of allergic asthma. Diesel particles might also play a role in the transmission of grass pollen allergens and thus become an extra asthma trigger. A variation in the mode of release of micronic particles occurs in other species, such as birch, where such particles are derived from burst birch pollen tubes. These particles are positive for Bet v 1 and are starch granules which are released into the atmosphere after light rain as a result of pollen germination on, e.g., leaves. After subsequent rupture of pollen tubes their contents are released when conditions become drier.
Similar content being viewed by others
Abbreviations
- DECP:
-
diesel exhaust carbon particles
- DMP:
-
2,2-dimethoxypropane
- GPC:
-
grass pollen count
- IgE:
-
immunoglobulin E
- IgG:
-
immunoglobulin G
- OGPS:
-
onset of the grass pollen season
References
Bates DV, Fish BR, Hatch TF, Mercer TT, Morrow PE (1966) Deposition and retention models for internal dosimetry of the human respiratory tract. Health Phys 12: 173–207
Becker WM, Darsow U, Behrendt H (1990) Effect of extracts of airborne particulate matter on grass pollenDactylis glomerata: allergen release and morphology. Allergologie 13: 443
Behrendt H, Becker WM, Friedrichs KH, Darsow U, Tomingas R (1992) Interaction between aeroallergens and airborne particulate matter. Int Arch Allergy Immunol 99: 425–428
Bellomo R, Gigliotti P, Treloar A, Holmes P, Suphioglu C, Singh MB, Knox RB (1992) Two consecutive thunderstorm associated epidemics of asthma in the city of Melbourne: the possible role of rye-grass pollen. Med J Aust 156: 834–837
Brostoff J, Hall T (1996) Hypersensitivity: type I. In: Roitt I, Brostoff J, Male D (eds) Immunology, 4th edn. Mosby, London, pp 212–217
Bruce CA, Norman PS, Rosenthal RR, Lichtenstein LM (1977) The role of ragweed pollen in autumnal asthma. J Allergy Clin Immunol 59: 449–459
Bufe A, Schramm G, Keown MB, Schlaak M, Becker W-M (1995) Major allergenPhl p Vb in timothy grass is a novel pollen RNase. FEBS Lett 363: 6–12
Busse WW, Reed CE, Hoehne JH (1972) Where is the allergic reaction in ragweed asthma? II. Demonstration of ragweed antigen in airborne particles smaller than pollen. J Allergy Clin Immunol 50: 289–293
Cosgrove DJ, Bedinger P, Durachko DM (1997) Group 1 allergens of rye-grass as cell wall-loosening agents. Proc Natl Acad Sci USA 94: 6559–6564
Desai R (1995) Oxygen enrichment of the diesel engine. PhD thesis, The University of Melbourne, Australia
Devalia JL, Rusznak C, Herdman MJ, Trigg CJ, Tarraf H, Davies RJ (1994) Effect of nitrogen dioxide and sulphur dioxide on airway response of mild asthmatic patients to allergen inhalation. Lancet 344: 1668–1671
Dockery DW, Pope CA III (1994) Acute respiratory effects of particulate air pollution. Annu Rev Public Health 15: 107–132
— —, Xu X-P (1993) An association between air pollution and mortality in six U.S. cities. N Engl J Med 329: 1753–1759
El-Ghazaly G, Takahashi Y, Nilsson S, Grafstroem E, Berggren B (1995) Orbicules inBetula pendula and their possible role in allergy. Grana 34: 300–304
Emberlin J (1995) Plant allergens on pauci-micronic airborne particles. Clin Exp Allergy 25: 202–205
Fischer S, Grote M, Fahlbusch B, Müller WD, Kraft D, Valenta R (1996) Characterisation of Phl p 4, a major timothy grass (Phleum pratense) pollen allergen. J Allergy Clin Immunol 98: 189–198
Freidhoff LR, Ehrlich-Kautzky E, Grant JH, Meyers DA, Marsh DG (1986) A study of the human response toLolium perenne (rye) pollen and its components, Lol p 1 and Lol p 2 (rye I and rye II). J Allergy Clin Immunol 78: 1190–1201
Griffith IJ, Smith P, Pollock I, Theerakulpisut P, Avjioglu A, Davies S, Hough T, Singh MB, Simpson RJ, Ward LD, Knox RB (1991) Cloning and sequencing ofLol p I, the major allergenic protein of ryegrass pollen. FEBS Lett 279: 210–215
Grote M, Dolecek C, Van Ree R, Valenta R (1994) Immunogold electron microscopic localization of timothy grass (Phleum pratense) pollen major allergens Phl p I and Phl p V after anhydrous fixation in acrolein vapor. J Histochem Cytochem 42: 427–431
—, Swoboda I, Meagher RB, Valenta R (1995) Localization of profilin- and actin-like immunoreactivity in in vitro-germinated tobacco pollen tubes by electron microscopy after special waterfree fixation techniques. Sex Plant Reprod 8: 180–186
Hidy GM (1984) Aerosols: an industrial and environmental science. Academic Press, Orlando
Hoehne JH, Reed CE (1971) Where is the allergic reaction in ragweed asthma? J Allergy Clin Immunol 48: 36–39
Kaeser W (1989) Freeze-substitution of plant tissue with a new medium containing dimethoxypropane. J Microsc 154: 273–278
Knox RB (1993) Grass pollen, thunderstorms and asthma. Clin Exp Allergy 23: 354–359
—, Suphioglu C (1996) Pollen allergens: development and function. Sex Plant Reprod 9: 318–323
- Tuohy M (1982) Pollen, plants and people: a review of pollen aerobiology in southern Australia. In: Proceedings of the 6th Australian Weeds Conference, 1981, vol 2, pp 125–142
—, Suphioglu C, Taylor PE, Desai R, Watson HC, Peng JL, Bursil LA (1997) Major grass pollen allergen Lol p 1 binds to diesel exhaust particles (DEPC): implications for asthma and air pollution. Clin Exp Allergy 27: 246–251
— — —, Ladiges P, Nelson G (1998) Pollen allergens: molecular and immunological analyses and implications for systematics. In: Owens S (ed) Reproductive biology in systematics, conservation and economic botany. Royal Botanic Gardens, Kew, pp 449–463
Miki-Hirosige H, Nakamura S, Yasueda H, Shida T, Takahashi Y (1994) Immunocytochemical localization of the allergenic proteins in the pollen ofCryptomeria japonica. Sex Plant Reprod 7: 95–100
Ong EK, Singh MB, Knox RB (1995a) Aeroallergens of plant origin: molecular basis and aerobiological signiflfcance. Aerobiologia 11: 219–229
— — — (1995b) Grass pollen in the atmosphere of Melbourne: seasonal distribution over nine years. Grana 34: 58–63
—, Taylor PE, Knox RB (1997) Forecasting the onset of the grass pollen season in Melbourne (Australia). Aerobiologia 13: 43–48
Ostro BD, Lipsett MJ, Wiener MB, Seiner JC (1991) Asthmatic responses to airborne acid aerosols. Am J Public Health 81: 694–702
Pacini E, Taylor PE, Singh MB, Knox RB (1992) Development of plastids in pollen and tapetum of rye-grass,Lolium perenne L. Ann Bot 70: 179–182
Pope CA III, Dockery DW (1992) Acute health effects of PM10 pollution on symptomatic and asymptomatic children. Am Rev Respir Dis 145: 1123–1128
— —, Spengler JD, Raizenne ME (1991) Respiratory health and PM10 pollution: a daily time series analysis. Am Rev Respir Dis 144: 666–674
Rantio-Lehtimaeki A, Viander M, Koivikko A (1994) Airborne birch pollen antigens in different particle sizes. Clin Exp Allergy 24: 23–28
Schäppi GF, Monn C, Wuthrich B, Wanner HU (1996) Direct determination of allergens in ambient aerosols: methodological aspects. Int Arch Allergy Immunol 110: 364–370
—, Suphioglu C, Taylor PE, Knox RB (1997a) Concentrations of the major birch tree allergen Bet v 1 in pollen and respirable fine particles in the atmosphere. J Allergy Clin Immunol 100: 656–661
—, Taylor PE, Staff IA, Suphioglu C, Knox RB (1997b) Source of Bet v 1 loaded inhalable particles from birch revealed. Sex Plant Reprod 10: 315–323
— —, Suphioglu C, Knox RB (1997c) A new approach to the investigation of allergenic respirable particles using a modified Anderson Impactor. Grana 36: 373–375
—, Kenrick J, Staff IA, Suphioglu C (1998) Predicting the grass pollen count from meteorological data with regard to estimating the severity of hayfever symptoms in Melbourne (Australia). Aerobiologia 14: 29–37
— —, Pain MC, Cameron PA, Dent AW, Staff IA, Suphioglu C (1999a) Concentrations of major grass group 5 allergens in pollen grains and atmospheric particles: implications for hayfever and allergic asthma sufferers sensitised to grass pollen allergens. Clin Exp Allergy 29: 633–641
— —, Staff IA, Rolland JM, Suphioglu C (1999b) Immunologie significance of respirable atmospheric starch granules containing major birch allergen Bet v 1. Allergy 54: 478–483
Shivanna KR, Heslop-Harrison J (1981) Membrane state and pollen viability. Ann Bot 70: 179–188
Singh MB, Hough T, Theerakulpisut P, Avjioglu A, Davies S, Smith PM, Taylor PE, Simpson R, Ward L, McClusky J, Puy R, Knox RB (1991) Isolation of cDNA encoding a newly identified major allergenic protein of rye-grass pollen: intracellular targetting to the amyloplast. Proc Natl Acad Sci USA 88: 1384–1388
—, Taylor PE, Knox RB (1993) Special preparation methods for immunocytochemistry of plant cells. In: Beesley JE (ed) Immuno-cytochemistry: a practical approach. IRL Press at Oxford University Press, Oxford, pp 77–102
Smart IJ, Knox RB (1979) Aerobiology of grass pollen in the city atmosphere of Melbourne: quantitative analysis of seasonal and diurnal changes. Aust J Bot 27: 317–331
—, Tuddenham WG, Knox RB (1979) Aerobiology of grass pollen in the city atmosphere of Melbourne: effects of weather parameters and pollen sources. Aust J Bot 27: 333–342
Smith MT (1991) Studies on the anhydrous fixation of dry seeds of lettuce (Lactuca sativa L.). New Phytol 119: 575–584
Smith P, Ong EK, Knox RB, Singh MB (1994) Immunological relationships among group I and group V allergens from grass pollen. Mol Immunol 31: 491–498
Solomon WR, Bürge HA, Muilenberg ML (1983) Allergen carriage by atmospheric aerosol. J Allergy Clin Immunol 72: 443–447
Spieksma FTM, Kramps JA, Van der Linden AC (1990) Evidence of grass pollen allergenic activity in the smaller micronic atmospheric aerosol fraction. Clin Exp Allergy 20: 273–280
—, Nikkels BH, Dijkman JH (1995) Seasonal appearance of grass pollen allergen in natural, pauci-micronic aerosol of various size fractions: relationship with airborne grass pollen concentration. Clin Exp Allergy 25: 234–239
Staff IA, Taylor PE, Smith P, Singh MB, Knox RB (1990) Cellular localization of water soluble, allergenic proteins in rye-grass (Lolium perenne) pollen using monoclonal and specific IgE antibodies with immunogold probes. Histochem J 22: 276–290
Suphioglu C, Singh MB, Taylor PE, Bellomo R, Holmes P, Puy R, Knox RB (1992) Mechanism of grass-pollen-induced asthma. Lancet 339: 569–572
Takafuji S, Suzuki S, Koizumi K, Tadokoro K, Ohashi H, Muranaka M, Miymoto T (1989) Enhancing effect of suspended particulate matter on the IgE antibody production in mice. Int Arch Allergy Appl Immunol 90: 1–7
Takahashi Y, Sakaguchi M, Inouye S, Miyazawa H, Imaoka K, Katagiri S (1991) Existence of exine-free airborne allergen particles of Japanese cedar (Cryptomeria japonica) pollen. Allergy 46: 588–593
Taylor PE, Singh MB, Knox RB (1993) Strategies for the localization of rapidly diffusible proteins in pollen. J Comput Assist Microsc 5: 53–56
—, Staff IA, Singh MB, Knox RB (1994) Localization of the two major allergens in rye-grass pollen using specific monoclonal antibodies and quantitative analysis of immunogold labelling. Histochem J 26: 392–401
Wilson AF, Novey HS, Berke RA, Surprenant EL (1973) Deposition of inhaled pollen extract in human airways. N Engl J Med 288: 1056–1060
Wüthrich B (1991) In Switzerland, pollinosis has really increased in the last decade. Allergy Clin Immunol News 3: 41–44
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Staff, I.A., Schäppi, G. & Taylor, P.E. Localisation of allergens in ryegrass pollen and in airborne micronic particles. Protoplasma 208, 47–57 (1999). https://doi.org/10.1007/BF01279074
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01279074