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Magnetite Biomineralization in the Human Brain (Iron/Extremely Low Frequency Magnetic Fields) JOSEPH L

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Magnetite Biomineralization in the Human Brain (Iron/Extremely Low Frequency Magnetic Fields) JOSEPH L Proc. Natl. Acad. Sci. USA Vol. 89, pp. 7683-7687, August 1992 Biophysics Magnetite biomineralization in the human brain (iron/extremely low frequency magnetic fields) JOSEPH L. KIRSCHVINK, ATSUKO KOBAYASHI-KIRSCHVINK, AND BARBARA J. WOODFORD* Division of Geological and Planetary Sciences, The California Institute of Technology, Pasadena, CA 91125 Communicated by Leon T. Silver, May 7, 1992 ABSTRACT Although the mineral magnetite (Fe3O4) is mollusks (12), arthropods (13), and chordates (14, 15) and is precipitated biochemically by bacteria, protists, and a variety suspected in many more groups (16). In the microorganisms of animals, it has not been documented previously in human (10, 11) and fish (15), linear chains of membrane-bound tissue. Using an ultrasensitive superconducting magnetometer crystals of magnetite (magnetosomes) form structures best in a clean-lab environment, we have detected the presence of described as "biological bar magnets." ferromagnetic material in a variety of tissues from the human We report here that human tissues possess similar crystals brain. Magnetic particle extracts from solubilized brain tissues of biogenic magnetite, with minimum estimates between 5 examined with high-resolution transmission electron micros- and 100 million single-domain crystals per gram in the tissues copy, electron diffraction, and elemental analyses identify of the human brain. Magnetic particle extracts from solubi- minerals in the magnetitemaghemite family, with many ofthe lized tissues examined with high-resolution transmission crystal morphologies and structures resembling strongly those electron microscopy (TEM) and electron diffraction identify precipitated by magnetotactic bacteria and fish. These mag- minerals in the magnetite-maghemite solid solution, with netic and high-resolution transmission electron microscopy many crystal morphologies and structures resembling those measurements imply the presence of a minimum of 5 million precipitated by magnetotactic bacteria and fish. single-domain crystals per gram for most tissues in the brain and >100 million crystals per gram for pia and dura. Magnetic property data indicate the crystals are in clumps of between 50 MATERIALS AND METHODS and 100 particles. Biogenic magnetite in the human brain may Tissue Samples. Human brain material was obtained 12-24 account for high-field saturation effects observed in the Ti and h postmortem from the Alzheimer's Disease Research Center T2 values of magnetic resonance imaging and, perhaps, for a Consortium of Southern California. Samples of brain and variety of biological effects of low-frequency magnetic fields. meninges were dissected using acid-cleaned ceramic or Tef- lon-coated instruments. These tissues were placed into 70% In past studies of iron storage and magnetic resonance ethanol [made with deionized water and filtered through a imaging (MRI), it has been assumed universally that there are 200-nm (pore-size) Millipore filter] in containers that had no permanently magnetized (ferromagnetic) materials pre- previously been cleaned with 2 M HCl. Samples from seven sent in human tissues (1, 2). Similar assumptions have been brains were obtained from patients whose ages averaged 65 made in virtually all biophysical assessments of human risk years and ranged from 48 to 88 years. Four ofthese were from associated with exposure to static and extremely low- suspected Alzheimer disease patients. Cerebral cortical areas frequency magnetic fields (3) and by critics (4) of epidemio- and cerebellum were included for all seven brains. In one logical studies that suggest links between weak power-line- case, brain and spinal dura, basal ganglia, and midbrain and, frequency magnetic fields and various human disorders (5, 6). in another case, olfactory bulbs, superior sagittal sinus, and These analyses have focused on the side effects of electrical tentorium of the dura were obtained in addition to the above induction or possible diamagnetic and paramagnetic interac- tissues. tions. However, the ferrimagnetic mineral magnetite (Fe3O4) Magnetometry. Subsamples for magnetic measurements is formed biochemically by many living organisms. Because were removed from the tissues by using similar tools in a ferromagnetic crystals interact more than a million times magnetically shielded dust-free clean laboratory (19). Mea- more strongly with external magnetic fields than do diamag- surements of materials were made a netic or paramagnetic materials of similar volume, earth- ferromagnetic using strength magnetic fields can yield many responses that stand magnetometer employing Rf-biased superconducting quan- above thermal noise (7). Hence, the assumption implicit in tum interference devices (SQUIDs), designed to measure the past studies that human tissues are free of ferromagnetic total ferromagnetic moment of samples placed within a material needs to be reassessed critically and tested experi- Helmholtz-coil pickup loop (20). Samples were fastened to a mentally. thin acid-washed monofilament string, and a stepping motor Previous searches for biogenic magnetite in human tissues moved the sample vertically between the magnetization and have not been conclusive (8, 9). Despite this, extensive demagnetization coils and the measurement region of the research over the past 30 years has demonstrated that many SQUID magnetometer. Several magnetic analyses borrowed organisms have the biochemical ability to precipitate the from the field of rock and mineral magnetism (21-23) were ferrimagnetic minerals magnetite (Fe3O4) (10-16) and greigite performed routinely on frozen tissue samples to determine (Fe3S4) (17). In terms of its phyletic distribution, magnetite the concentration, mineralogy, and packing geometry of any biomineralization is particularly widespread, having been ferromagnetic materials present. documented in monerans (10), protists (11), and animals (12-16), with a fossil record extending back into Precambrian Abbreviations: MRI, magnetic resonance imaging; SQUID, super- time (18). Within Kingdom Animalia, it is known within the conducting quantum interference device; TEM, transmission elec- tron microscopy; IRM, isothermal remanent magnetization; ARM, anhysteretic remanent magnetization. The publication costs of this article were defrayed in part by page charge *Present address: Department of Anatomy and Cell Biology, Uni- payment. This article must therefore be hereby marked "advertisement" versity of Southern California, 1333 San Pablo Street, Los Angeles, in accordance with 18 U.S.C. §1734 solely to indicate this fact. CA 90033. 7683 Downloaded by guest on September 24, 2021 7684 Biophysics: Kirschvink et al. Proc. Natl. Acad. Sci. USA 89 (1992) Sample Preparation for the Magnetometer. Pia and blood ments were made by indexing the spot patterns produced by vessels were removed from all samples of the meninges selected-area electron diffraction on individual mineral grains before analysis in the SQUID magnetometer. Two prepara- and on rings from powder patterns, with calibration against tion methods were used. Large intact samples ofthe cerebral a gold film standard. An estimate ofthe grain-size distribution cortex and cerebellum were frozen directly in liquid nitrogen. was made by measuring the length and width of 70 crystal Brain tissues that fractured upon freezing or dissection were shadows from a large clump. Control samples consisting of placed into a previously acid-cleaned ice-cube mold and the solutions without brain tissues, as well as the solutions frozen into blocks with small quantities of nonmagnetic spiked with known quantities ofbacterial magnetite, were run deionized water. Either the frozen piece of brain or the to check for contaminants in the solvents as well as to ice/brain block was attached by a slip knot to the monofil- determine their effect, ifany, on the well-studied morphology ament line and then centered within the column ofthe SQUID of bacterial magnetites. magnetometer. Background instrument noise and the levels of laboratory contaminants were monitored with blank 15-g RESULTS ice cubes of distilled deionized water; typical ice-cube back- ground noise levels were in the range of 2 x 10-8 A m2 kg-1. Magnetometry. All of the tissues examined had isothermal All aqueous solutions used in sample handling were passed remanent magnetizations (IRMs) that saturated in applied through 200-nm filters. All solutions, including the toluene fields of -300 mT, a characteristic property ofthe magnetite- and tissue solubilizers, were cleaned magnetically by storing maghemite series. The ability to gain and lose remanent for at least 2 weeks prior to use in containers with large magnetization in these experiments is a definitive character- high-intensity NdFeB magnets strapped to their base to aid in istic of ferromagnetic materials. Table 1 shows the mean the removal of any preexisting ferromagnetic contaminants. values for each brain. The average magnetization indicates Extraction and Electron Microscopy. Extraction devices the equivalent of =4 ng of magnetite per gram of tissue. In made from Pyrex weighing vials were used to remove the contrast, average values for the meninges from three brains magnetic particles from the brain tissues. The ground-glass (Table 1) are nearly 20 times higher, or -70 ng/g. For caps were modified by glass blowing to make a thin-walled comparison, measurements of IRM from triple-distilled cylindrical finger, sealed on the bottom, extending from the deionized ice cubes yield a background "noise"
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